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Multicriteria-based ranking for risk management of food-borne parasites: report of a Joint FAO/WHO expert meeting, 3-7 September 2012, FAO Headquarters, Rome, Italy.

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M I C R O B I O L O G I C A L

R I S K

A S S E S S M E N T

S E R I E S

23 Multicriteria-based ranking for risk management of food-borne parasites

ISSN 1726-5274

M I C R O B I O L O G I C A L

R I S K

A S S E S S M E N T

S E R I E S

23 Multicriteria-based ranking for risk management of food-borne parasites

Report of a Joint FAO/WHO Expert Meeting, 3–7 September 2012, FAO Headquarters, Rome, Italy

Food and Agriculture Organization of the United Nations World Health Organization 2014

The designations employed and the presentation of material in this information product do not imply the expression of any opinion whatsoever on the part of the Food and Agriculture Organization of the United Nations (FAO) or of the World Health Organization (WHO) concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. The mention of specific companies or products of manufacturers, whether or not these have been patented, does not imply that these are or have been endorsed or recommended by FAO or WHO in preference to others of a similar nature that are not mentioned. All reasonable precautions have been taken by FAO and WHO to verify the information contained in this publication. However, the published material is being distributed without warranty of any kind, either expressed or implied. The responsibility for the interpretation and use of the material lies with the reader. In no event shall FAO and WHO be liable for damages arising from its use.

WHO Library Cataloguing-in-Publication Data: Multicriteria-based ranking for risk management of food-borne parasites: report of a Joint FAO/ WHO Expert Meeting, 3-7 September 2012, FAO Headquarters, Rome, Italy. 1.Food contamination. 2.Food parasitology. 3.Parasites. 4.Risk management – methods. I.World Health Organization. II.Food and Agriculture Organization of the United Nations. ISBN 978 92 4 156470 0 (WHO) ISBN 978-92-5-108199-0 (print) (FAO) E-ISBN 978-92-5-108200-3 (PDF) (FAO) ISSN 1726-5274 (NLM classification: WA 701)

Recommended citation: FAO/WHO [Food and Agriculture Organization of the United Nations/World Health Organization]. 2014. Multicriteria-based ranking for risk management of food-borne parasites. Microbiological Risk Assessment Series No. 23. Rome. 302pp FAO and WHO encourage the use, reproduction and dissemination of material in this information product. Except where otherwise indicated, material may be copied, downloaded and printed for private study, research and teaching purposes, or for use in non-commercial products or services, provided that appropriate acknowledgement of FAO and WHO as the source and copyright holder is given and that their endorsement of users’ views, products or services is not implied in any way. All requests for translation and adaptation rights, and for resale and other commercial use rights should be made via www.fao.org/contact-us/licencerequest or addressed to copyright@fao.org. FAO information products are available on the FAO website (www.fao.org/publications) and can be purchased through publications-sales@fao.org. © FAO/WHO 2014

Contents Acknowledgments Contributors Abbreviations used in the report Executive Summary x xi xiv xv

1 Background 2 Objectives and approach

1 4 7 7 8 11 12 13 14

2.1 Identi cation of parasites 2.2 De nition of primary and secondary parasite and food pathways 2.3 De nition of criteria for parasite scoring 2.4 Scoring parasites according to criteria 2.5 De nition of criteria weights 2.6 Calculation of parasite scores

3 Results

3.1 The global ranking of food-borne parasites 3.2 Trade scores for the ranked parasites 3.3 Socio-economic impacts for the ranked parasites 3.4 Conclusions 14 18 20 23 23 24 26 32 35

4 Risk management options for the higher ranked parasites 4.1 General risk management considerations 4.2 Generic risk management options 4.3 Some speci c considerations for risk management

Conclusions and recommendations References

ANNEXES

Annex 1 Identi cation of food-borne parasites for consideration Annex 2 Food-borne parasite ranking exercise: summary card Annex 3 Food-borne parasite ranking exercise form: explanation of criteria Criterion No. 1. Number of global food-borne illnesses Criterion No. 2. Geographical distribution (endemic regions) Criterion No. 3. Acute Morbidity Severity Criterion No. 4. Chronic Morbidity Severity Criterion No. 5. Fraction chronic Criterion No. 6. Mortality rate Criterion No. 7. Increasing trend in disease Criterion No. 8. International trade Criterion No. 9. Distributional impacts (socio-economic impact) Criterion No. 10. Quality of evidence Comments References

40 44 45 45 46 47 48 49 50 50 50 51 52 52 52 53 54 62 63 63 63 63 64 65 65 65 66 66 67 67 68 68 68 69 70 70 70 70

Annex 4. Criteria weights worksheet Annex 5. Sensitivity analysis Annex 6. Risk management actions Annex 7. Speci c information for the ranked parasites A7.1 Anisakidae and anisakiasis General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.2 Ascaris spp. General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations Other relevant information References A7.3 Balantidium coli General information Geographical distribution Disease

Trade relevance Impact on economically vulnerable populations References A7.4 Cryptosporidium spp. General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.5 Cyclospora cayetanensis General information Geographical distribution Disease Trade relevance and impact on economically vulnerable populations References A7.6 Diphyllobothrium spp. General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations Other relevant information References A7.7 Echinococcus granulosus General information Geographical distribution Disease Trade relevance of cystic echinococcosis Impact of CE on economically vulnerable populations References A7.8 Echinococcus multilocularis General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.9 Entamoeba histolytica General information Geographical distribution Disease Trade relevance

71 71 71 72 72 73 74 74 74 75 77 77 78 78 79 79 82 82 82 83 84 84 84 84 88 88 89 89 90 91 92 95 95 95 96 97 98 98 101 101 101 101 102

Impact on economically vulnerable populations References A7.10 Fasciola spp. General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.11 Giardia duodenalis General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.12 Heterophyidae and heterophyidiasis General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations Other relevant information References A7.13 Opisthorchiidae General information Geographical distribution (endemic regions) Disease Trade relevance Impact on economically vulnerable populations Other relevant information References A7.14 Paragonimus spp. General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.15 Sarcocystis spp. General information Geographical distribution Prevalence in food animals Prevalence in humans

102 102 104 104 104 104 105 105 106 108 108 108 108 110 110 110 112 112 112 112 113 113 113 114 115 115 115 115 117 117 117 117 119 119 119 120 122 122 122 124 124 124 124 125

Disease Trade relevance Impact on economically vulnerable populations References A7.16 Spirometra spp. General information Geographical distribution Disease Trade relevance and impact on vulnerable populations References A7.17 Taenia saginata General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.18 Taenia solium General information on the parasite Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.19 Toxocara spp. General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.20 Toxoplasma gondii General Information Geographical distribution Disease Trade relevance and Impact on economically vulnerable populations References A7.21 Trichinella spp. other than T. spiralis General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References

126 126 126 127 129 129 129 130 130 131 133 133 133 134 135 135 135 137 137 137 137 138 138 139 141 141 141 142 143 143 143 145 145 146 147 149 149 152 152 152 153 154 154 154 vii

A7.22 Trichinella spiralis General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations Other relevant information References A7.23 Trichuris trichiura General information Geographical distribution Disease Trade relevance Impact on economically vulnerable populations References A7.24 Trypanosoma cruzi General information Geographical distribution Disease Chagas disease by oral transmission Trade relevance Impact on economically vulnerable populations References A7.25 Glossary of Parasitological Terms

156 156 156 156 157 158 158 158 160 160 160 160 161 161 161 163 163 163 164 164 165 165 165 167 171 172 172 172 179 179 179 180 182 182 182 182 184 187 190 190 218 218 218

Annex 8. Regional Reports Annex 8.1 – Africa A8.1.1 Introduction A8.1.2 Data availability in humans, and food attribution A8.1.3 Agri-food trade A8.1.4 Consumer perception A8.1.5 Social sensitivity A8.1.6 Risk management Annex 8.2 – Asia A8.2.1 Introduction A8.2.2 Description of individual foodborne parasitic diseases A8.2.2.1 Meat-borne parasite infections A8.2.2.2 Fish- and shell sh-borne parasites A8.2.2.3 Plant (fruit and vegetable)-borne parasites A8.2.3 Risk management strategies A8.2.4 Sources consulted Annex 8.3 – Australia A8.3.1 Preparation A8.3.2 Data availability in humans and food attribution

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A8.3.3 Agri-food trade A8.3.4 Consumer perception A8.3.5 Social sensitivity A8.3.6 Risk management A8.3.7 Sources cited in the discussion Annex 8.4 – Europe A8.4.1 Preparation A8.4.2 Data availability in humans and food attribution A8.4.3 Data on the burden of disease and food attribution A8.4.4 Data on parasite prevalence, incidence and concentration in the main food categories A8.4.5 Agri-food trade A8.4.6 Consumer perception A8.4.7 Social sensitivity A8.4.8 Risk management A8.4.9 Sources cited in the text of the Europe section discussion Annex 8.5 – Near East A8.5.1 Compilation of data availability on food borne parasites relevant to the Near East A8.5.2 Agri-food trade A8.5.3 Consumer perception and social sensitivity A8.5.4 Risk management A8.5.5 Sources cited in the discussion Annex 8.6 – North America with notes on Central America A8.6.1 Report preparation A8.6.2 Data availability on human occurrences and food attribution A8.6.3 Data on the burden of disease and food attribution A8.6.4 Agri-food trade A8.6.5 Consumer perception A8.7.6 Social sensitivity A8.6.7 Risk management Annex 8.7 – South America A8.7.1 Report preparation A8.7.2 Data availability in humans and food attribution A8.7.3 Agri-food trade A8.7.4 Consumer perception A8.7.5 Social sensitivity A8.7.6 Risk management

226 227 227 228 228 230 230 230 231 231 231 233 234 235 235 249 249 250 250 251 251 267 267 267 267 267 268 268 268 268 268 268 268 268 287 287

Acknowledgments e Food and Agriculture Organization of the United Nations and the World Health Organization would like to express their appreciation to all those who contributed to the preparation of this report through their participation in the expert meeting and the provision of their time, expertise, data and other relevant information both before and a er the meeting. Special appreciation is extended to Mr Michael Batz for his work on the design and facilitation of the multicriteria-based ranking exercise, and to Dr Andrijana Rajic for her valuable help, particularly in the design and implementation of the pre-meeting activities, as well as the meeting approach. All contributors are listed on the following pages. Appreciation is also extended to all those who responded to the calls for data that were issued by FAO and WHO, and brought to our attention data in o cial documentation or not readily available in the mainstream literature. Final editing for language and preparation for publication was by Lawrence. orgeir

Contributors EXPERTS Pascal Boireau, Director, Laboratory for Animal Health, Maisons Alfort, 23 av. du Général de Gaulle, BP 67, 94703 Maisons-Alfort, France. Jorge E. Bolpe, Head, Departamento de Zoonosis Rurales de Azul, Ministerio de Salud de la Provincia de Buenos Aires, Calle España Nº 770 (7300) Azul, Provincia de Buenos Aires Argentina. Allal Dakkak, Professor, Parasitology Unit, Department of Pathology and Veterinary Public Health, OIE Reference Laboratory for Echinococcsis/Hydatidosis, Institut Agronomique et Veterinaire Hassan II., B.P. 6202 Rabat-Instituts, Morocco. Brent Dixon, Head, Food-borne Viruses, Parasites and Other Disease Agents, Microbiology Research Division, Bureau of Microbial Hazards, Food Directorate, HPFB, Health Canada, Ottawa, Ontario, Canada. Ronald Fayer, Senior Scientist, United States Department of Agriculture, Agricultural Research Service, Environmental Microbial and Food Safety Laboratory, Beltsville, Maryland 20705, USA. Jorge E. Gómez Marín, Director, Centro de Investigaciones Biomédicas de la Universidad del Quindio, Avenida Bolívar 12N, Código Postal 630004, Armenia, Colombia. Erastus Kang’ethe, Professor, Department of Public Health, Pharmacology and Toxicology, University of Nairobi, Kenya. Malcolm Kennedy, Professor, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, Scotland, UK. Samson Mukaratirwa, Professor and Head, School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X54001, Durban 4000, South Africa. K. Darwin Murrell, Adjunct Professor, WHO/FAO Collaborating Centre for Emerging Parasitic Zoonoses, Danish Centre for Experimental Parasitology, Department of Veterinary Disease Biology, Faculty of Life Sciences, University of Copenhagen, Frederiksberg, Denmark. Tomoyoshi Nozaki, Director, Department of Parasitology, National Institute of Infectious Diseases, 1-23-1 Toyama, Shinjuku, Tokyo 162-8640, Japan.

Ynés Ortega, Associate Professor, Center for Food Safety, University of Georgia, 1109 Experiment St., Gri n, GA 30223, USA. Subhash C. Parija, Professor and Head, Department of Microbiology, Jawaharlal Institute of Post-graduate Medical Education and Research, Puducherry 605 006, India. Lucy Robertson, Professor, Parasitology Laboratory, Section for Microbiology, Immunology and Parasitology, Institute for Food Safety and Infection Biology, Norwegian School of Veterinary Science, PO Box 8146 Dep, 0033 Oslo, Norway. Mohammad Bagher Rokni, Department of Medical Parasitology and Mycology, School of Public Health and Institute of Public Health Research, Tehran University of Medical Sciences, Iran. Patrizia Rossi, Senior Research Scientist, Unit of Gastroenteric and Tissue Parasitic Diseases, Department of Infectious, Parasitic and Immunomediated Diseases, Istituto Superiore di Sanita. Viale Regina Elena 299, 00161 Rome, Italy. Said Shalaby, Research Professor and Chairman, Department. of Research and Application of Complementary Medicine Medical Division, National Research Center, Cairo, Egypt. Paiboon Sithithaworn, Professor, Department of Parasitology and Liver Fluke and Cholangiocarcinoma Research Centre, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, ailand. Rebecca Traub, Senior Lecturer, Veterinary Public Health, School of Veterinary Sciences, University of Queensland, Australia. Nguyen van De, Professor, Department of Parasitology, Hanoi Medical University, Viet Nam. Joke W.B. van der Giessen, Director, National Reference Laboratory for Foodborne Parasites, National Institute of Public Health and the Environment (RIVM), Laboratory for Zoonoses and Environmental Microbiology, Antonie van Leeuwenhoeklaan 9, P.O. Box 1,3720 BA Bilthoven, e Netherlands.

RESOURCE PERSONS Michael Batz, Head of Food Safety Programs, Emerging Pathogens Institute, University of Florida, Gainesville, USA. Annamaria Bruno, Joint FAO/WHO Food Standards Programme, Codex Secretariat, Rome. Verna Carolissen, Joint FAO/WHO Food Standards Programme, Codex Secretariat, Rome.

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Steve Hathaway, Director, Science and Risk Assessment Standards Branch, Ministry of Agriculture and Forestry, Pastoral House 25, PO Box 2526, Wellington 6140, New Zealand. Iddya Karunasagar, Fisheries and Aquaculture Department, Food and Agriculture Organization of the United Nations. Gillian Mylrea, Deputy Head, Department of International Trade, OIE World Organisation for Animal Health, 12, Rue de Prony, 75017 Paris, France. Patrick Otto, Animal Production and Health Division, Food and Agriculture Organization of the United Nations. Edoardo Pozio, Director, Unit of Gastroenteric and Tissue Parasitic Diseases, Department of Infectious, Parasitic and Immunomediated Diseases, Istituto Superiore di Sanita, Viale Regina Elena 299, 00161 Rome, Italy. Andrijana Rajic, Nutrition and Consumer Protection Division, Food and Agriculture Organization of the United Nations.

SECRETARIAT Sarah Cahill, Nutrition and Consumer Protection Division, Food and Agriculture Organization of the United Nations. Marisa Caipo, Nutrition and Consumer Protection Division, Food and Agriculture Organization of the United Nations. Mina Kojima, Department of Food Safety and Zoonoses , World Health Organization. Simone Magnino, Department of Food Safety and Zoonoses , World Health Organization. Kaye Wachsmuth, International Public Health Consultant, PO Box 4488, DeLand, FL 32721, USA.

DECLARATIONS OF INTEREST All participants completed a Declaration of Interests form in advance of the meeting. None were considered to present any potential con ict of interest.

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Abbreviations used in the report CAC CCFH FAO FERG GAP GHP HACCP OIE WHO Codex Alimentarius Commission Codex Committee on Food Hygiene Food and Agriculture Organization of the United Nations WHO Food-borne Disease Epidemiology Reference Group Good Agricultural Practice Good Hygiene Practice Hazard Analysis and Critical Control Points World Organisation for Animal Health World Health Organization

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Executive Summary At the 42nd Session (December 2010) of the Codex Committee on Food Hygiene (CCFH), the Committee requested that FAO and WHO “review the current status of knowledge on parasites in food and their public health and trade impact in order to provide CCFH with advice and guidance on the parasite-commodity combinations of particular concern, issues that need to be addressed by risk managers, and the options available to them.” On the basis of this information, CCFH would determine the feasibility of developing general guidance as a framework for annexes that would address speci c parasite-commodity combinations. To address this request FAO and WHO initiated a series of activities that culminated in an expert meeting on 3–7 September 2012. Preceding the meeting, relevant data were identi ed and collated through a formal “call-for-data” and by written reports from experts representing the African, Asian, Australian, European, Near Eastern, North American and South American Regions. Some 93 potential parasites were initially identi ed for consideration. Preliminary work was also undertaken on the development of a ranking tool and experts provided inputs to this through an on-line questionnaire. is preliminary ranking work combined with additional discussions during the meeting, resulted in a list of 24 parasites for ranking. Experts further identi ed speci c vehicles of transmission for each of the 24 parasites. It is important to note that food-borne parasitic diseases present some unique challenges, and are o en referred to as neglected diseases. Noti cation to public health authorities is not compulsory for most parasitic diseases, and therefore o cial reports do not re ect the true prevalence or incidence of the disease occurrences (under-reporting). e parasites have complicated life cycles, which may include multiple hosts, some of which could become food, or the parasites themselves could contaminate food. e disease can present with prolonged incubation periods (up to several years), be sub-clinical or asymptomatic, and epidemiological studies associating illness with a speci c food type may not be possible. With technical guidance, the experts de ned global criteria for evaluating the 24 food-borne parasites and rated each parasite along these criteria. e criteria can be summarized as: (1) number of global illnesses; (2) global distribution; (3) morxv

bidity-acute; (4) morbidity-chronic; (5) percentage chronic; (6) mortality; (7) increasing illness potential; (8) trade relevance; and (9) socio-economic impact. Each criterion was then weighted by the experts in terms of their importance. e three criteria for disease severity (3, 4 and 5) were combined into one criterion, giving a total of 7 criteria weights, re ecting the relative importance of each criterion to the overall score. e overall score for each parasite was calculated by normalized parasite criteria scores multiplied by fractional weights, and summed. e primary outputs of the expert meeting were the development of the ranking tool and the actual global ranking, based primarily on public health concerns, i.e. 85% of weighting. e global ranking of food-borne parasites by “importance” and their primary food vehicle in descending order was: Taenia solium – Pork Echinococcus granulosus – Fresh produce Echinococcus multilocularis – Fresh produce Toxoplasma gondii – Meat from small ruminants, pork, beef, game (red meat and organs) Cryptosporidium spp. – Fresh produce, fruit juice, milk Entamoeba histolytica – Fresh produce Trichinella spiralis – Pork Opisthorchiidae – Freshwater sh Ascaris spp. – Fresh produce Trypanosoma cruzi – Fruit juices Giardia duodenalis – Fresh produce Fasciola spp. – Fresh produce (aquatic plants) Cyclospora cayetanensis – Berries, fresh produce Paragonimus spp. – Freshwater crustaceans Trichuris trichiura – Fresh produce Trichinella spp. – Game meat (wild boar, crocodile, bear, walrus, etc.) Anisakidae – Salt water sh, crustaceans, and cephalopods Balantidium coli – Fresh produce Taenia saginata – Beef Toxocara spp. – Fresh produce Sarcocystis spp. – Beef and pork Heterophyidae – Fresh and brackish water sh Diphyllobothriidae – Fresh and salt water sh Spirometra spp. – Fish, reptiles and amphibians xvi

is ranking should be considered a “snapshot” and representative only of the information available at the time, the criteria used for ranking, and the weightings assigned to those criteria. Also, some of these parasites had very similar rankings, so it might be more relevant to consider the parasites in groups of concern, e.g. top 5, or top 10, rather than the individual ranking position. With more information or with changing human and animal behaviour, and with climate change e ects, parasite scoring and subsequent ranking could also change. As with many phases of risk analysis, it may be important to repeat and update the process on a regular basis. In fact, with heavily weighted public health criteria, the ranking results in part re ect risk de ned as a function of the probability of an adverse health e ect, and the severity of that e ect consequential to a hazard in food. If the parasites are ranked only on trade criteria scores, the order of importance changes: Trichinella spiralis, Taenia solium, Taenia saginata, Anisakidae and Cyclospora cayetanensis are the top ve. In this way, individual criteria can be considered, e.g. by CCFH, outside of the total scoring and weighting processes to assure that speci c concerns can be addressed transparently and separately if needed. Since criteria weights were calculated separately from the individual parasite scoring, alternative weighting schemes re ecting the judgments of risk managers could be used to generate alternative ranking, using the scoring of the parasites undertaken by the expert meeting. us, the ranking process that was developed was considered to be as important an output of the meeting as the ranking result, since it allows the global ranking to be updated through changes in scoring and to re ect the priorities of di erent groups of risk managers or stakeholders through di erent weighting. e process can be completely re-run at national or regional level using data more speci c to that particular country or region. Finally, the meeting also highlighted some considerations for risk management including possible approaches for the control of some of these food-borne parasites. Reference is also made to existing risk management texts as appropriate. is information, together with the global ranking of the parasites, the identi cation of the primary food vehicles and information on food attribution, is aimed to assist Codex in terms of establishing their priorities and determining the next steps in terms of managing these hazards. However, it should be noted that management of speci c parasites may then require further scienti c input, which it was not feasible to provide as part of this present process.

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1 Background Infectious diseases caused by food-borne parasites, generally de ned as “ Any organism that lives in or on another organism without bene ting the host organism; commonly refers to pathogens, most commonly in reference to protozoans and helminths.” CDC, NO DATE

are o en referred to as neglected diseases, and from the food safety perspective parasites have not received the same level of attention as other food-borne biological and chemical hazards. Nevertheless, they cause a high burden of disease in humans. e infections may have prolonged, severe, and sometimes, fatal outcomes, and result in considerable hardship in terms of food safety, security, quality of life, and negative impacts on livelihoods. Food-borne parasites can be transmitted by ingesting fresh or processed foods that have been contaminated with the transmission stages (spores, cysts, oocysts, ova, larval and encysted stages) via the environment; by animals (o en from their faeces); or by people (o en due to inadequate hygiene). Food-borne parasites can also be transmitted through the consumption of raw and under-cooked or poorly processed meat and o al from domesticated animals, wild game and sh containing infective tissue stages (Sli o, Smith and Rose, 2000). Despite the fact that the parasite does not replicate outside a live host, food processing techniques in common use can arti cially amplify the quantity of contaminated food that reaches the consumer, increasing the number of human cases (e.g. sausage made from meats of di erent origin). CHAPTER 1 BACKGROUND

Noti cation to public health authorities is not compulsory for most parasitic diseases, and therefore o cial reports do not re ect the true prevalence or incidence of the disease (under-reporting) that occurs. Although the global impact of food-borne diseases on public health is largely unknown due to limited data, the burden of disease caused by some parasites has been estimated by the WHO Foodborne Disease Epidemiology Reference Group (FERG). FERG (Fürst, Keiser and Utzinger, 2012) assessed the global burden of human food-borne trematodiasis with data for the year 2005, and estimated that 56.2 million people were infected by food-borne trematodes, of which 7.8 million su ered from severe sequelae and 7158 died worldwide. is and other FERG papers include individual parasites and country data, as well as disability calculations, but reports do not routinely provide food attribution data. e complexities of the epidemiology and life cycle of each parasite play a central role in the identi cation, prevention and control of the risks associated with foodborne parasitic diseases. Surveillance for parasitic diseases is complicated by the o en prolonged incubation periods, sub-clinical nature and unrecognized, chronic sequelae. e spread of food-borne parasitic diseases is enhanced by changes in human behaviour, demographics, environment, climate, land use and trade, among other drivers. (Orlandi et al., 2002; Macpherson, 2005; Broglia and Kapel, 2011). Some examples worth mentioning in the context of this report are the globalization of food trade, which o ers new opportunities for dissemination; variations in food preferences and consumption patterns, such as the expected global increase in meat consumption in emerging countries over the next 20 years; the increasing tendency to eat meat, sh or seafood raw, under-cooked, smoked, pickled or dried; or the demand for exotic foods such as bush meat or wild game. e impact of climate change on parasite life cycles in the environment will depend on several factors, such as the number of hosts (one, two or more) involved in the transmission, the presence or absence of intermediate hosts or vectors, free living stages1 and reservoir host species (Mas-Coma, Valero and Bargues, 2009; Polley and ompson, 2009). e potential for climate change could a ect parasite host(s) habitats, present a greater likelihood of contamination due to extreme weather events, and create increased pressure on some food sources (Davidson et al., 2011). Options for control of some parasites that can cause human and zoonotic diseases have been addressed collaboratively by FAO, WHO and the World Organisation for Animal Health (OIE). Extensive guidelines for the surveillance, management, prevention and control of taeniosis/cysticercosis and trichinellosis have been published in 2005 and 2007, respectively, and OIE is currently revising the chapter in the Terrestrial Animal Health Code for Trichinella spp., Echinococcus granulosus 1

For the purposes of food-borne animal parasite discussions, a free-living stage is a stage of a parasite that lives outside of its host or hosts (Rohr et al., 2011).

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

and Echinococcus multilocularis. Aquaculture product standards are addressed by the Codex Alimentarius Commission (CAC) and the FAO Fisheries and Aquaculture Department. EU directives for food-borne parasites already exist. However, increased multidisciplinary collaboration is needed for risk-based prevention and control of parasites at all stages of the production-to-consumption continuum. Such control is necessary to safeguard public health and minimize production problems and economic losses caused by parasites. One of the CAC committees, the Codex Committee on Food Hygiene (CCFH), is currently developing “Guidelines for the Control of Speci c Zoonotic Parasites in Meat: Trichinella spiralis and Cysticercus bovis2”, working in close cooperation with OIE. In undertaking this work the Committee recognized the need to address food-borne parasites more broadly, based on their risk to human health as well as their socio-economic and trade impacts, and, if needed, to provide more general guidance for their control. erefore, at its 42nd Session (December 2010) the Committee requested that FAO and WHO “ review the current status of knowledge on parasites in food and their public health and trade impact in order to provide the CCFH with advice and guidance on the parasite-commodity combinations of particular concern, the issues that need to be addressed by risk managers, and the options available to them.” On the basis of this information, CCFH would evaluate the feasibility of developing a general guidance document that would provide a framework where annexes could address speci c parasite×commodity combinations. FAO and WHO convened an Expert Meeting on Food-borne Parasites on 3–7 September 2012 at FAO Headquarters, Rome, Italy, to respond to the request of the CCFH.

Clari cation note to the CCFH: During the expert meeting, the more precise taxonomic term Taenia saginata was used instead of the older and less formal designation, Cysticercus bovis. e human disease is taeniasis due to the tapeworm form, while the cattle disease is cysticercosis due to the metacestode (cysticercus) form (Flisser, Craig and Ito, 2011).

CHAPTER 1 BACKGROUND

2 Objectives and approach e objectives of the meeting were as follows: • • • To develop a ranked list of food-borne parasites of global importance. To identify the foods of greatest concern for the most important foodborne parasites. To provide an overview of the risk management options and approaches available for the control of the most highly ranked food-borne parasites. A systematic, evidence-based approach was taken to prioritize the food-borne parasites of global importance. An expert-based, multicriteria ranking tool was designed, and implemented during the meeting. It built on data gathered in advance of the meeting by means of an FAO/WHO formal “call for data” and through electronic working procedures facilitated by the FAO/WHO Secretariat. Additional data came from detailed presentations at the meeting itself. Results of this ranking exercise achieved the rst objective and informed systematic discussions to address the second and third objectives. e meeting was attended by 21 internationally recognized experts in food-borne parasites from 20 countries covering all global regions, together with 9 resource people and the FAO/WHO secretariat, as well as additional resource people from FAO and WHO (see list of Contributors in the front matter). e expert meeting was chaired by Dr Joke van der Giessen, Dr Brent Dixon served as Vice-Chair and Dr Rebecca Traub served as Rapporteur.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

e process used to rank food-borne parasites and identify risk management strategies is shown in Figure 1. e process comprised 6 primary steps: (1) Identi cation of parasites for ranking; (2) Identi cation of key foods of concern for each parasite; (3) Identi cation and de nition of criteria by which each parasite would be evaluated; (4) Expert scoring of each parasite based on the criteria; (5) Weight importance of each criterion in overall parasite scoring; and (6) Calculation of parasite scores and subsequent ranking. As shown in the gure, some steps can be further broken down into stages, many of which began prior to the meeting. e gure also shows which activities in the process were primarily conducted by the FAO/WHO secretariat and which were done entirely by experts or by experts with FAO/WHO facilitation. e expert-based parasite ranking exercise was developed following a multicriteria assessment (MCA) approach. It was speci cally based on a number of similar assessments conducted for zoonotic and infectious diseases in the past few years (e.g. Anderson et al., 2011; Cardoen et al., 2009; Havelaar et al., 2010; Humblet et al., 2012; Krause et al., 2008; Ng and Sargeant, 2012). Most of these ranking approaches follow a similar multicriteria approach in which a set of hazards are evaluated with a set of criteria, including but not limited to public health, and then overall scores are computed based on a weighting of those criteria. ere is no standard methodology for conducting a multicriteria assessment, however, as such ranking exercises are designed for speci c risk management contexts, they are inevitably constrained by resources, time and data availability. e multicriteria-based ranking process included a number of e orts to collect, collate and share data and acquired knowledge. Published information was collected from the peer reviewed literature. is included the publications from the FERG Parasitic Diseases Task Force, FAO/WHO/OIE guidelines and others. In the 2011 call for data, FAO and WHO requested information on (1) impact of food-borne parasitic diseases; (1A) impact on public health and (1B) socioeconomic impact; (2) monitoring and inspection systems; (3) control and management; (4) risk assessment and risk pro les; and (5) risk ranking. Twenty-two member countries and one regional body (EU) responded. Results showed that most had adopted surveillance systems for food-borne parasitic diseases (n=20); monitoring and inspection systems for food-borne parasites (n=15); and appropriate control and management measures (n=15). However, data or information, or both, on socio-economic impact, were very limited, as were risk assessments, pro les and ranking. Most of the respondents recognized that Trichinella, Cryptosporidium, Echinococcus, Giardia, Toxoplasma and Taenia were important as foodborne pathogens.

CHAPTER 2 OBJECTIVES AND APPROACH

PRIOR TO MEETING Call for data & country responses

LEGEND FAO/WHO Secretariat Expert panel

Complete parasite list

Dra parasite screening

Final parasite screening

Online questionnaire

Parasite/food pairs

Initial food categories scheme Written regional reports

Final food categories

Expert parasite scoring

Regional presentations

Dra criteria

Finalize criteria Weight criteria Parasite overall score calculation & ranking

Risk management recommendations FIGURE 1. Flow chart of the multicriteria ranking exercise

Written reports were produced in advance of the meeting for each of seven geographic regions: Africa, Asia, Paci c (only included Australia), Europe, Near East, North America and South America. Presentations based on these reports were made by the experts at the meeting. e regional reports considered the current overall quantity and quality of data at the regional and global levels; burden of disease and food attribution; data on parasite prevalence, incidence and concentration in the main food categories; agri-food trade; consumer perception; social sensitivity; and risk management options. ese reports were used by the experts in their deliberations during the meeting (see Annex 8 of this report). An online questionnaire was sent to the 21 experts to examine the importance of criteria by which parasites might be evaluated and to elicit experts’ initial judgments on the global and regional importance of each of 93 parasites. e questionnaire also captured information about the background and expertise of each expert. 6

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

2.1 IDENTIFICATION OF PARASITES Following a “call for data” (July 2011) and input from experts, a comprehensive list of 93 parasites was created. is list was intended to capture the global set of human parasites for which consumption of food may be a relevant pathway. An online questionnaire (July 2012) was sent to experts and each expert was asked to score the global and regional importance of each parasite from “not important” to “very important.” It was decided that scoring 93 parasites was beyond the scope of the meeting, so results from these scores were used to create a three-tiered initial prioritization of parasites (Table A1 in Annex 1). is initial prioritization was then used by experts in a screening exercise conducted at the meeting. Led by the Chair and Vice-Chair, experts reduced the parasite list by using inclusion and exclusion criteria. First, parasites were grouped by species or genera (Table A1.2 in Annex 1); then, where applicable, based on common transmission routes, clinical manifestations and attributable food-borne sources. Parasites were excluded when the proportion of food-borne illnesses was negligible or when parasites were only relevant in a limited geographic area (Table A1.3 in Annex 1). e result was a nal list of 24 parasites to be ranked.

2.2 DEFINITION OF PRIMARY AND SECONDARY PARASITE AND FOOD PATHWAYS In order to characterize primary food-borne pathways for key parasites, an eightcategory food scheme was developed and incorporated into regional written reports generated by experts prior to the meeting. In their reports, experts identied speci c foods within these categories and provided references to support food associations. ese categories were created to capture both food animal reservoirs and hosts, as well as foods contaminated within the food chain (such as produce contaminated by water). Following discussion at the meeting, consensus was reached among the experts on a food scheme comprising ve broad categories (land animals; aquatic animals; dairy products; plants; and other) and seventeen sub-categories. is scheme is shown in Table 1. is scheme was then applied to each of the 24 parasites, and used to identify the primary food vehicles associated with each parasite. For some parasites, secondary food vehicles were also de ned, as shown in Table 2.

CHAPTER 2 OBJECTIVES AND APPROACH

TABLE 1. Food category scheme Food category Land animals Food subcategory Beef Pork Poultry Small ruminants Other meat Game and wild animals Aquatic animals Marine sh Freshwater sh Shell sh Aquatic mammals Dairy products Plants Dairy products Berries Fruit juices Other fruit Leafy greens Other vegetables Fresh produce (refers to 2 or more of the above) Other Other foods

2.3 DEFINITION OF CRITERIA FOR PARASITE SCORING Based on previous prioritization studies and risk management needs, ve categories were considered for the analysis: public health, microbial ecology, animal health, agribusiness and trade, and socio-economic impact. A number of potential criteria in these categories were included in the online questionnaire to appraise the applicability of these criteria and to elicit experts’ judgment on which criteria were more important. is information was used to generate an expansive list of 41 potential criteria in these ve categories. e FAO/WHO Secretariat narrowed the list of potential criteria to 11 and presented these to the experts at the meeting. Following extensive discussions on the list of criteria, consensus was reached on a nal list of 9 criteria. Of these criteria, 5 relate to the quantity and severity of global disease, while two others relate to the global distribution of these illnesses and the potential for short-term emergence of increased disease. e remaining two criteria relate to the potential for the parasite (in its primary and secondary foods, de ned previously) to a ect trade, and the impact of the parasite on economically vulnerable communities. 8 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

TABLE 2. Parasites and main food vehicles Secondary food vehicles Global food attribution (1) All food-borne ( sh).

Parasites

Anisakidae

Primary food category Aquatic animals

Ascaris spp.

Plants

Primary food vehicles Marine sh, crustaceans and cephalopods Fresh produce

Plants

Fresh produce

Food-borne association but proportion unknown Mainly soilborne (geophagic). Multiple exposure routes in endemic areas. (2) Food-borne association but proportion unknown.

Balantidium coli Cryptosporidium spp.

Plants

Cyclospora cayetanensis All food-borne.

Plants

Food-borne association but proportion unknown (Estimated to be 8% in USA (Scallan et al,, 2011). Food-borne outbreaks documented. Water may be most important route. Mostly food-borne, e.g. basil, berries, lettuce, etc.

Diphyllobothriidae

Aquatic animals

Plants Fresh produce

Fresh produce, fruit juice, milk Berries, fresh produce Fish (freshwater and marine) Fresh produce

Food-borne association but proportion unknown.(3)

Echinococcus granulosus Echinococcus multilocularis Fresh produce

Plants

Plants Entamoeba histolytica (Older studies did not distinguish Entamoeba histolytica from E. dispar.) Plants Fasciola spp. Fresh produce (aquatic plants) Fresh produce Molluscan shell sh

Food-borne association but proportion unknown. Epidemiological risk surveys suggest food is not major transmission route.(4) Food-borne association but proportion unknown. Waterborne route important. Hygiene and food handlers o en implicated.

CHAPTER 2 OBJECTIVES AND APPROACH

Giardia duodenalis (syn. G. intestinalis, G. lamblia)

Plants

Heterophyidae

Aquatic animals

Mainly food-borne through aquatic plants. Outbreaks reported. Food-borne association but proportion unknown. Food-borne outbreaks documented. Handlers and multiple food types implicated (Christmas pudding, etc.). Water-borne outbreaks reported. All food-borne ( sh). All food-borne ( sh).

Opisthorchiidae

Aquatic animals

Fresh- and brackish-water sh Freshwater sh

10 Primary food vehicles Global food attribution (1) All food-borne. Pork All food-borne All food-borne. Taeniosis exclusively meatborne. All food-borne for S. suihominis and S. bovihominis Freshwater crustacea Beef Frog, snake meat Beef Pork Fresh produce Secondary food vehicles Fresh produce Meat from small Fresh produce, ruminants, pork, seafood, dairy beef, game meat (red products meat and organs) Pork Horse, Game meat Pork Game meat (5) Fresh produce Fruit juices Taeniosis exclusively meatborne. Food-borne association but proportion unknown. Cysticercosis mainly soilborne; contaminated plants may be signi cant in some regions. Food-borne association but proportion unknown. Mainly soilborne (geophagy). Food-borne association (fresh produce) but proportion unknown. Multiple routes of infection, but transmission through meat is important. (Meatborne Toxoplasma infections estimated to be 22% in USA, Boyer et al., 2011; 53% in Chile, Muñoz et al., 2010; 26% in Colombia, López et al., 2005) Waterborne outbreaks documented. Exclusively meatborne. Making sausage or similar food products increases the risk to the consumer from a single animal. Exclusively meatborne. Food-borne association but proportion unknown. Mainly soilborne. Food-borne outbreaks documented. Fruit juice in limited geographic area. Mainly transmitted by insects

Parasites

Primary food category

Aquatic animals

Land animals

Other

Paragonimus spp. Sarcocystis spp. Sparganosis – Spirometra spp. Taenia saginata Taenia solium

Land animals

Land animals Plants (cysticercosis)

Toxocara spp.

Plants

Toxoplasma gondii

Land animals

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Trichinella spiralis

Land animals

Trichinella spp. (other than Land animals Trichinella spiralis) Plants Trichuris trichiura

Trypanosoma cruzi

Plants

Notes: (1) The information in this column is based on peer reviewed publications in the scienti c literature, unpublished reports and expert opinion, which may be the only approach to estimate food attribution for some of the parasitic diseases on a global basis. (2) Ascaris spp. eggs can become ubiquitous in an endemic area, making attribution di cult if not impossible. (3) The incubation period for Echinococcus granulosus can be as long as 5 to 15 years; it is not possible to precisely identify an exposure occurring many years previously. However, there are many articles indicating that E. granulosus eggs contaminate plants, and evidence that people in the endemic, developing countries consume vegetables, including raw. It is almost impossible to pinpoint the food source because the transmission routes are varied (e.g. contact with dog, other canids (fox, wolf), soil, etc.). (4) The incubation period for Echinococcus multilocularis can be 5–15 years, and the disease, alveolar echinococcus, is diagnosed at an advanced stage; it is not possible to precisely identify an exposure occurring many years previously. (5) Wild boar, crocodile, bear, walrus, etc.

e nal criteria selected for scoring were: (1) Number of global food-borne illnesses (manifesting disease); (2) Global distribution (number of regions); (3) Acute morbidity severity (disability weight); (4) Chronic morbidity severity (disability weight); (5) Fraction of illness that is chronic (%); (6) Case-fatality ratio (%); (7) Likelihood of increased human burden (%); (8) How relevant is this parasite-food pathway for international trade?; and (9) What is the scope of the impact on economically vulnerable communities? For each of these 9 criteria, between three and ve scoring levels were de ned. For 7 criteria, these scoring levels were de ned quantitatively, while the remaining two were qualitative. Scoring levels were intended to allow for appropriate di erentiation among the 24 parasites. ese criteria, along with a question pertaining to data quality, are shown in Annex 2. Note that question 8, on international trade concerns, relates speci cally to the pathogen in its primary food vehicle, whereas all other questions refer to the parasite in general.

2.4 SCORING PARASITES ACCORDING TO CRITERIA Experts were divided into ve groups of 4 to 5 people, organized so that each group had, to the extent possible, coverage across regions and expertise. Each group was given three documents: a summary card form for each parasite (see Annex 2), a document explaining each criterion and how to score it (Annex 3), and a list of parasites. e lists of parasites provided to each group were staggered in order to maintain equal numbers of scores across parasites, because all groups were unlikely to complete summary cards for all 24 parasites. Each group used available material, such as regional written reports, published literature and WHO material on disability weights, coupled with online searches, to facilitate a discussion of each criterion for each parasite. Each group scored a summary card for each parasite on their list. Preliminary criteria scores were tabulated into spreadsheets for each group, and preliminary scores were presented back to the group. Discussions around large disparities in preliminary scores allowed the group to identify some di erences in interpreting criteria. Once the expert panel reached consensus and greater clarity and agreement on criteria de nitions, groups re-convened to review their scores. Following a second tabulation of preliminary results and similar discussion on criteria de nitions, a third round of scoring was conducted to obtain nal group parasite criteria scores. Ultimately, two groups scored all 24 parasites and the remaining groups scored 21, 18 and 14 parasites respectively. us, 11 parasites had 5 sets of criteria scores, 7 parasites had 4 sets of scores, and 6 parasites had 3 sets of scores.

CHAPTER 2 OBJECTIVES AND APPROACH

2.5 DEFINITION OF CRITERIA WEIGHTS In multicriteria assessment, individual criterion scores are combined into an overall score for each parasite. In this instance, each criterion score was rst normalized to a 0–1 scale, with equal divisions among levels. To combine these criteria scores, each criterion was weighted as a fraction of the total score, with all weights summing to 100%. TABLE 3. Mean of elicited criteria weights used in the multi-criteria ranking. Scoring criterion Criterion weight

W1. W2. W345. W6. W7. W8. W9.

Number of global food-borne illnesses Global distribution Morbidity severity Case-fatality ratio Increasing illness potential Trade relevance Impacts on economically vulnerable communities

0.22 0.14 0.22 0.15 0.07 0.10 0.10

In this approach, each criterion is assigned its own weight, though in this case, three criteria relating to the severity of disease morbidity were combined (3, severity weight for acute disease; 4, severity weight for chronic disease; and 5, fraction of disease that is chronic) into a single adjusted criterion. Details are explained in the next section, but this combination resulted in requiring a single weight for morbidity severity, shown in Table 3 as W345. us, although there are 9 criteria used to compute the overall score for each parasite, there are only 7 criteria weights. A worksheet (Annex 4) was given to each group and to six from the FAO/WHO Secretariat. Table 3 presents the mean criteria weights across all participants. Criteria weights re ect the relative importance of the individual criterion in the overall score. Table 3 shows that public health criteria had most in uence on the outcome of the ranking, accounting for 80% of the total weights agreed by experts. In particular, disease severity (morbidity severity and case-fatality ratio) accounted for 39% of the total score. ese average expert criteria weights were incorporated into the ranking model. Because criteria weights are calculated separately from individual parasite scoring, alternative weighting schemes re ecting the judgments of risk managers or stakeholders could be used to generate alternative rankings that nevertheless are based on expert parasite criteria scores.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

2.6 CALCULATION OF PARASITE SCORES e overall score for each parasite is given by the following equation: Score = C1*W1+C2*W2+{C3*(1-C5)+C4*C5}*W345+C6*W6+C7*W7+C8*W8 +C9*W9 where C are parasite-speci c normalized criteria scores and W are constant criteria weights that are the same for all parasites. Criteria 3, 4 and 5 are combined to produce a single morbidity criteria; it is essentially the weighted average of acute and chronic disease severity. us, criteria 3, 4 and 5 have one associated weight, denoted in the equation as W345. Otherwise the calculation is straightforward: normalized parasite criteria scores are multiplied by fractional weights, and summed. Overall scores therefore range from 0 to 1. A spreadsheet model was developed to calculate overall scores for each parasite based on all group summary cards and averaged criteria weights. e resulting scores were then ranked to produce the current list of global food-borne parasites.

CHAPTER 2 OBJECTIVES AND APPROACH

3 Results 3.1 THE GLOBAL RANKING OF FOOD BORNE PARASITES e results of the ranking exercise, where the top ranking parasites are arranged on the x-axis from le to right in decreasing rank order and the average weights (in percentage) on the y-axis, are presented in Figure 2. is gure was obtained from the average of all elicited weights for the criteria. Among the top ranked parasites are those that have already been singled out by WHO as neglected tropical diseases (NTD), and identi ed by FERG as priorities for further burden of illness studies. As noted in Chapter 2, this ranking is a combination of scoring the parasites based on prede ned criteria and weighting the criteria based on the importance assigned to them by the expert meeting participants. Since many of the criteria were public health related, there were not big di erences between the nal ranking and the outcome of the scoring exercise alone, where all criteria are considered to have equal weight. Sensitivity analysis was carried out using alternative criteria weighting schemes (see Annex 5). Figure A5.3 in Annex 5 compares the ranks for global foodborne parasites scored across alternative criteria weighting schemes. Figure A5.5 in Annex 5 presents the scores for the public health criteria only, weighted equally, compared with baseline ranking based on all criteria and elicited weights. ese gures are included for reference and indicate that the top 4 parasites remain the same based on expert scoring. It is also interesting to note that the gradually declining trend along the x-axis from le to right remains generally the same. erefore the weighting of criteria did not radically change the ranks, 14 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Taenia solium Echinococcus granulosus Echinococcus multilocularis Toxoplasma gondii Cryptosporidium spp. Entamoeba histolytica Trichinella spiralis Opisthorchiidae Ascaris spp. Trypanosoma cruzi Giardia duodenalis Fasciola spp. Cyclospora cayetanensis Paragonimus spp. Trichuris trichiura Trichinella spp.* Anisakidae Balantidium coli Taenia saginata Toxocara spp. Sarcocystis spp. Heterophyidae Diphyllobothriidae Spirometra spp. 0.00 10.00 20.00 30.00 40.00 50.00 60.00 70.00 80.00

Normalized overall score

FIGURE 2. Global ranking of food-borne parasites using a multicriteria ranking tool for scoring parasites, with weighting of scoring criteria based on criteria scores and weights elicited from expert meeting participants (Note: Trichinella spp.* includes Trichinella species except T. spiralis).

and the public health criteria alone were not so di erent from the expert ranking. is also re ects the dominance of public health-related criteria in the ranking tool. A short overview of the top 8 parasites in the above ranking is provided below. Further information relevant to the management of these parasites is provided in Chapter 4. As risk managers consider individual parasites, there will be a need to go into more depth for each. Speci c information on the 24 ranked parasites was generated a er the meeting and can be found in Annex 7. Taenia solium Taenia solium (ranked 1st in Figure 2) is estimated to infect millions of persons worldwide. It is unique in that the larval or cysticercus stage can infect humans 15

CHAPTER 3 RESULTS

as well as pigs, and can cause a wide range of debilitating neurological problems, including epilepsy. Human cysticercosis o en occurs in areas where traditional pig husbandry is practiced, and is endemic in the Andean area of South America, Brazil, Central America and Mexico, China, India, Southeast Asia, and sub-Saharan Africa. e disease can be spread by poor sanitation and hygiene and improper slaughterhouse services. Human neurocysticercosis is increasingly being reported in developed countries, possibly due to increases in globalization and immigration (Carabin et al., 2011). Echinococcus granulosus and E. multilocularis In a recent report on neglected tropical diseases, scientists stated for Echinococcus granulosus and E. multilocularis (ranked 2nd and 3rd in Figure 2): “ e diseases caused by these parasites represent a substantial burden on the human population. Present estimates suggest that cystic hydatid disease, caused by Echinococcus granulosus, results in the loss of 1 to 3 million disability-adjusted life years per annum. e annual cost of treating cases and economic losses to the livestock industry probably amount to US$ 2 billion. Alveolar echinococcosis, caused by E. multilocularis, results in the loss of about 650 000 disability-adjusted life years per year. ese diseases are perhaps some of the more important global parasitic diseases, with more than 1 million people a ected at any one time, many showing severe clinical syndromes.” WHO, 2011

Toxoplasma gondii Toxoplasma gondii is capable of infecting virtually all warm blooded animals, including humans. It has been estimated that close to 30% of the world population may be infected by Toxoplasma gondii. Pregnant women and immunocompromised individuals are the main risk groups, although immune-competent persons may develop ocular disease as a result of an infection later on in life. Furthermore, T. gondii infection has been associated with behavioural changes and development of psychiatric disorders. e parasite may be transmitted trans-placentally to the foetus when T. gondii infections occur during pregnancy. is can result in foetal death, central nervous system abnormalities or eye disease, a ecting the child throughout its lifetime. e two routes of food-borne infection—via tissue cysts in various types of meat or organs, or via oocysts contaminating a wide range of food vehicles—makes transmission control a challenge. Cryptosporidium spp. e importance of Cryptosporidium spp. as a food-borne parasite has emerged in part through outbreak investigations that have linked fresh produce, fruit juice 16 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

and dairy products with disease. In the USA, it is estimated that 8% of the annual food-borne disease burden may be attributed to this parasite. For most people, symptomatic cryptosporidiosis is characterized by acute watery diarrhoea, o en accompanied by abdominal pain, nausea or vomiting, low grade fever, headache and general malaise. Most patients recover within 2–3 weeks, but highly immunocompromised patients may su er chronic illness, also leading to severe disease and sometimes death. For most parasitic infections there is some treatment available, but for Cryptosporidium spp. infections in the immunocompromised, there is none. ere is also increasing evidence that cryptosporidiosis may have long-term e ects, such as chronic gastrointestinal conditions. In addition, it is noted that cryptosporidium oocysts are very resistant to chlorine commonly used to treat water. Entamoeba histolytica Entamoeba histolytica, as with Cryptosporidium spp., is probably primarily transmitted through food handlers and contaminated water, which can enter the food chain causing illnesses attributed to fresh produce; it should be noted that, unlike some Cryptosporidium spp., E. histolytica is not zoonotic. Amoebiasis is traditionally limited to dysenteric-like symptoms, with abdominal pain, bloody or mucoid diarrhoea, and tenesmus, but has the ability to invade extra-intestinal tissues also, e.g. inducing liver abscesses, and extra-hepatic spread of E. histolytica is associated with relatively high mortality (20–75%). One of the problems with its detection is that microscopy methods used for E. histolytica do not di erentiate it from nonpathogenic species. is parasitic disease is of importance globally, but occurs predominately in developing countries and may be transmitted with immigrant populations to developed areas. Unlike Cryptosporidium spp., E. histolytica is susceptible to chlorine. Trichinella spiralis Trichinella spiralis, like all Trichinella species, has a unique lifecycle in that there is no environmental transmission stage – thus all cases are due to ingestion of meat containing the encysted larvae; meat types typically associated with T. spiralis include pork, horse meat, and game. Globally, there were 65 818 human infections reported between 1986 and 2009, with most of these reported for hospitalized patients in Romania, where 42 patient deaths were reported. However, there may be increased exposure through human behavioural trends, e.g. consumption of raw horse meat, dog meat, wild boar, and other sylvatic animal meats, as well as practices of free-range animal husbandry (infected animals are asymptomatic). Opisthorchiidae e Opisthorchiidae family includes various digenean parasites, of which the most medically important are Clonorchis sinensis, Opisthorchis viverrini and Opisthorchis CHAPTER 3 RESULTS

felineus. All are transmitted to humans via ingestion of the encysted metacercaria in the esh or skin of freshwater sh. Opisthorchiasis/clonorchiasis occurs autochthonously in southeast Asia, eastern Europe, and central Asia. FERG reported over 8 million infections globally in 2005, almost all of which occurred in southeast Asia, where over 300 000 people were heavily infected and 1323 died. Disabilityadjusted life years was 74 367. e FERG report further states that awareness of this food-borne problem is limited; only Japan and South Korea have established successful control programmes for sh-borne trematodiases. Opisthorchiasis is particularly worrisome in its potential to be carcinogenic; case-control studies have suggested that a substantial proportion of cholangiocarcinoma in some Asian countries can be due to infection with O. viverrini. Summary e fact that this is a global ranking may mean that some diseases that are severe and o en fatal, but limited to a particular region, are not highly ranked. One example is Chagas disease, transmission of which is at present largely restricted to parts of Central and South America, with FERG reporting over 11 000 deaths due to Trypanosoma cruzi worldwide in 2004. However, survival of the trypomastigotes in fruits and juices might present an unknown risk for global dissemination in the world market. e parasites currently being considered by the CCFH were ranked seventh (T. spiralis) and nineteenth (T. saginata/C. bovis) for overall importance by the experts.

3.2 TRADE SCORES FOR THE RANKED PARASITES e data used to rank parasites and generate Figure 2 are used to produce Figure 3, in which only the average trade criteria scores for each parasite are displayed. is gure suggests that there may be additional or separate trade issues that could be considered by risk managers such as Codex and national food authorities. e parasites currently contemplated by the CCFH, T. spiralis and T saginata/C. bovis, were considered among the most important for trade, based on criteria scores. In the regional reports, Trichinella spiralis, Taenia saginata, Taenia solium and/or Echinococcus granulosus were mentioned as current or potential trade concerns in the African, Australian, European, Near Eastern and South American Regions. e North American and Asian Regions did not address this issue directly. It may be of interest to risk managers that the Anisakidae that ranked lower (17th) in overall importance, scored higher for the trade criteria, and were mentioned in

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Average criterion score (0-2)

FIGURE 3. Relative ranking of international trade importance of parasites in primary

food vehicles: average expert scores for Criterion 8 (based on Table 2; Trichinella spp.* includes all Trichinella species except T. spiralis)

CHAPTER 3 RESULTS

several country reports as a class of organisms important to the country. probably countries that trade or consume sh extensively.

ese are

Conversely, parasites of concern in the overall ranking may not rank high as a trade concern. An example is Toxoplasma gondii, which might be prevalent in meat products but is microscopic and does not a ect the appearance of the products, and there is no rapid, inexpensive, accurate test available. erefore, for trade purposes, it would be ranked lower than the easily visible and detectable parasites.

3.3 SOCIO ECONOMIC IMPACTS FOR THE RANKED PARASITES e data analysed to rank parasites and generate Figure 2 are also used to produce Figure 4, which presents average scores for the socio-economic impact criterion. e gure indicates that there may be additional or separate socio-economic concerns not addressed in the overall ranking or in trade issues. An example of this is Cyclospora cayetanensis, which may require further investigation. It is probable that this re ects the known and on-going, socio-economic impacts on Guatemalan berry farmers, following the relatively extensive outbreaks of cyclosporiasis in North America during the 1990s. Outbreaks were primarily associated with berries imported from Guatemala. Diseases caused by Taenia solium (ranked 1st) and Echinococcus granulosus and E. multilocularis (ranked 3rd and 4th, respectively) contribute to economic losses in human and animal populations in many parts of the world. ey are considered preventable diseases that can be controlled or eliminated and should be prioritized (Carabin et al., 2005). Stigmatization and social isolation, attached to the occurrence of epilepsy caused by neurocysticercosis (T. solium infection), are examples of societal impact presented in the African Regional report, that are di cult to quantify but add to the socio-economic burden of this disease. e parasites currently contemplated by the CCFH, T. spiralis and T. saginata/C. bovis were not considered important in terms of the socio-economic criterion.

3.4 CONCLUSIONS e ranking exercise has provided a picture of the food-borne parasites of global importance today and has created a seemingly useful tool that is transparent and reproducible. e tool can be used with emphasis on di erent criteria and with or without weight factors. It is imperative that future use of this ranking tool and

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Average criterion score (0-3)

FIGURE 4. Relative ranking of socio-economic impacts of parasites to vulnerable communities: average expert scores for Criterion 9 (based on Table 2; Trichinella spp.* includes all Trichinella species except T. spiralis)

CHAPTER 3 RESULTS

strategy be undertaken in a transparent manner. By using this approach, the results can be compared when the procedure is repeated. e experts ranked the most important parasites by using multicriteria analysis during the meeting. e results shown in Figure 2 indicate that the method clearly de nes those parasites that are highly ranked and those considered of lower rank. While Taenia solium clearly came out on top, there were less marked di erences between the parasites that ranked second, third and fourth. Similarly those that ranked h, sixth and seventh are very close together, suggesting that the individual ranking is less important than the overall picture that the ranking provides in terms of food-borne parasites. As noted in the explanation of the weighting of the criteria, public health importance was the primary driver of ranking, with almost equal importance being given to illness and severity. is importance given to severity will have contributed to the high ranking of Echinococcus granulosus, ranked second, followed by E. multilocularis. Toxoplasma gondii ranked fourth. e predominant disease burden of this parasite is con ned mainly to substantial risks in pregnancy to the unborn, and in immunocompromised people (e.g. HIV/AIDS, transplantation patients). However, acquired toxoplasmosis also may contribute also an additional, substantial disease burden; many uncertainties still exist. e ranking order is a ected by data availability; in the absence of data, or when data is limited, it is more di cult to categorize a parasite×food commodity. New data may in uence ranking order. For example, the increasing number of papers linking toxoplasmosis with chronic illness (Havelaar et al., 2012), including mental illness (Henriquez et al., 2009) may push this parasite further up the ranking in the near future. erefore, the parasite ranking list developed here should not be considered to be absolute or static; in order to remain current and t for purpose, it must be updated periodically. e tool can be used also for prioritizing regional and national agendas for policy or research activities. ere may be more speci c data at national or regional level, as well as di ering judgments on the importance of the various criteria, which could lead to a di erent ranking at a local level.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

4 Risk management options for the higher ranked parasites e identi cation of ranked parasites in Figure 2 is based not only on scienti c evidence where available (including both published and unpublished data), but also on expert experience and opinion, and is weighted primarily by the public health concerns of the experts. e ranking of parasites by overall importance is the primary input to the risk managers in CCFH, who will then consider other issues relevant to management priorities and actions. e ranking approach used in the expert meeting can be applied at the national level, where scoring may change, based on data availability and where weights may be placed on di erent criteria, based on the national situation or risk management issue. Risk managers need to ensure that aspects other than the initial ranking by the experts that need to be considered in the decision-making process should also be evidence-based where possible, and done in a transparent manner. is section outlines some of these other considerations.

4.1 GENERAL RISK MANAGEMENT CONSIDERATIONS It is important to recognize at all levels—global, regional and local—that there is a signi cant lack of information regarding food attribution for many parasitic diseases (Table 2). is is especially true for parasitic infections in which there may CHAPTER 4 RISK MANAGEMENT OPTIONS FOR THE HIGHER RANKED PARASITE

be a prolonged period (possibly many years) before symptoms appear (e.g. Echinococcus spp.) or those producing a chronic progression of disease (Ascaris spp., Trypanosoma cruzi and Trichuris trichiura). Food may be an important vehicle of transmission, but these parasites are not considered to be exclusively food-borne. For example, food may not be the primary transmission vehicle for Echinococcus spp.; however, the experts still considered these parasites as potential food-borne risks and advocate that further evidence be gathered to close this knowledge gap. Echinococcus granulosus and E. multilocularis ranked 2nd and 3rd, respectively, based largely on the potential severity of their associated diseases.

4.2 GENERIC RISK MANAGEMENT OPTIONS As with other food-borne biological hazards, there are some generic good practices that are relevant for the control of food-borne parasites but are not necessarily unique to parasites. e importance of such practices may therefore already be captured in various existing risk-management documents. However, the recognition of parasites as being somewhat neglected warrants mention of any relevant control measures and management options.

4.2.1

Primary production and pre-harvest

While many of the parasites of concern are meat or sh-borne, for many others the entry into the food chain is via water or soil, or both. For example, Ascaris, Cryptosporidium, Cyclospora, Echinococcus and Giardia are essentially transmitted through the faecal-oral route, but may be transmitted by contaminated water during primary production of foods such as fresh produce. us, the primary production and pre-harvest stage of the food chain are critical in terms of control of numerous parasites, and it was considered that parasites may not be adequately considered in Good Agriculture Practices (GAPs). Some important considerations are highlighted here. Parasites transmitted by the faecal-oral route Given the importance of the faecal-oral route of transmission for some parasites, areas for cultivation of fresh produce, particularly for raw consumption, need to be assessed in terms of their susceptibility to faecal contamination, whether from run-o from wild animals, farm animals, domestic animals or and humans, and the necessary measures taken to manage the identi ed risk. e importance of on-farm sanitation and hygiene in interrupting the life cycle of parasites and minimizing the opportunity for the faecal-oral route of transmission needs to be recognized, with appropriate installation and use of the relevant facilities promoted, e.g. functional on-farm latrines, and adequate hand-washing facilities.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

e use of organic fertilizer, particularly on produce, should be monitored closely in order to ensure that it is composted adequately to destroy parasite transmission stages prior to use. However, it should be noted that the e ectiveness of composting in destroying or inactivating parasites is uncertain, and should be considered a knowledge gap. Zoonotic parasites For those parasites with an indirect life cycle, special consideration must be given to breaking the cycle at the level of the intermediate host, such as snail (intermediate host) control in the case of trematode parasites in aquaculture. e role of dogs and cats (domestic or feral) in transmission of certain parasites needs to be highlighted and farmers and other relevant stakeholders educated on good practices, e.g. no feeding of raw or untreated carcasses or o al of livestock and sh to domestic dogs and cats, or allowing wild canids and felids access to dead livestock, aborted foetuses, etc., and sh products; population control of semi-domesticated, stray or feral dogs and cats in close vicinity to the farm or aquaculture ponds. Mass treatment of reservoir hosts, such as livestock, at frequent intervals in a sustainable fashion should ensure reduction in environmental contamination of infective stages. is applies to dogs in the case of echinococcosis by Echinococcus granulosus. Water is an important vehicle for transmission for a number of food-borne parasites. us attention to water quality throughout the food-chain, from primary production through processing to consumption is very important. Although not speci c to primary production, monitoring and surveillance were considered to be important tools in the control of parasites, and for complete effectiveness may need to begin at the pre-harvest stage. For example, the ability to trace back infected animals at the abattoir level will allow identi cation of ‘high risk’ animals or sh populations or regions, and help allocation and targeting of resources for control. Furthermore, the ability to trace back fresh produce to the country, and even farm, of origin will allow identi cation of ‘high risk’ regions for subsequent risk management decisions. Monitoring and surveillance programmes can identify potentially emerging trends and risks for regional incursion (displaced forest animals or hosts in expanding urban environments).

4.2.2 Post-harvest While post-harvest opportunities for control will be very dependent on the commodity of concern, it was considered that current Good Hygiene Practice (GHP), and HACCP plans for processing, etc., might not address parasitic hazards adequately. CHAPTER 4 RISK MANAGEMENT OPTIONS FOR THE HIGHER RANKED PARASITE

In terms of processing, many parasite stages in meat and sh are susceptible to freezing as a process step and to controlled cooking at the process and consumer levels. However, the time×temperature combinations can be important, and in the cases of some parasites, such as E. multilocularis eggs, lower temperature domestic freezing may not be adequate. Irradiation can be an e ective control measure and guidelines are available for its use in the control of Toxoplasma and Trichinella. Other control measures such as curing, salting, drying and high pressure processing need evaluation for speci c parasites and food commodity contexts. Vacuum packing and chilling do not alter the viability of parasites in meat (e.g. Toxoplasma tissue cysts in meat).

4.2.3 Education Education and awareness raising was identi ed as an important component of food-borne parasite control, and in some cases may be the only feasible option available. Education should be directed to actors throughout the food chain from farm and abattoir workers to food handlers (consumers and food retail outlets), and should address the gamut from good animal husbandry practices to hygiene and sanitation measures. In terms of consumer education there may also be a need to address speci c high risk population groups. For consumers, especially those who are pregnant or immunocompromised (e.g. individuals with HIV/AIDS), advice on the preparation and consumption of high risk foods such as fresh produce and tubers, carrots etc., adequate cooking of meat and sh prior to consumption and the importance of hygiene, e.g. hand-washing, is critical.

4.3 SOME SPECIFIC CONSIDERATIONS FOR RISK MANAGEMENT During the meeting speci c consideration was given to the management of the eight top ranked parasites, and some of the important aspects for consideration by risk managers in deciding how to address these parasites. ese considerations for Taenia solium, Echinococcus granulosus, E. multilocularis, Toxoplasma gondii, Cryptosporidium spp., Entamoeba histolytica, Trichinella spiralis and the Opisthorchiidae family are summarized in Table 4. Where they were identi ed, details of existing risk management texts or guidelines are provided. It should be noted that providing more speci c input on the top eight ranked parasites was a function of the time available at the expert meeting rather than any technical consideration. In addition, Table 5 provides some information on the global trade in those commodities identi ed as primary vehicles for the ranked parasites, thus providing an overview of their importance.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

TABLE 4. Some speci c risk management considerations relating to the top eight ranked parasites

Parasite

Hosts and main transmission routes – Food chains of concern Severity of illness Taeniosis – a relatively benign disease. Cysticercosis a severe, potentially fatal, infection Classi ed as eradicable but expensive and challenging to control. Human host means behaviour important in transmission Control strategies linked to whether a geographic area is categorized high or low risk Not complicated to control but requires coordination among relevant authorities. E ective treatment of dogs needs con nement and incineration of faeces for 2 days post treatment, then repeat in 45 days. Elimination of the parasite in dogs. Education of farmers to minimize on-farm contamination and infection of animals. Control of water used, including fruit and vegetable production. Sheep and/ or dog vaccination may be a future option. Vaccine use and chemo-therapeutic control in pigs. Good pig husbandry practices critical for sustainable control. Safe application of manure to control environmental contamination. Maintain high water quality. Safe slaughter practices and an e ective inspection system. Food handler education to target personal hygiene.

Examples of management options and challenges along the food Overarching chain factors for consideration in Post-harvest or Retail and risk management On-farm processing consumer

Examples of risk management texts and guidance

Taenia solium

Two transmission routes: Undercooked pork – adult tapeworm infection (taeniosis) T. solium eggs – environment (e.g. via fresh produce) – larval stage infection (cysticercosis)

FAO/WHO/OIE Consumer 2005. education on the role of humans in transmission. Consumption of raw produce in endemic areas is high risk. Cooking is e ective.

CHAPTER 4 RISK MANAGEMENT OPTIONS FOR THE HIGHER RANKED PARASITE

Echinococcus granulosus

Fresh produce Sheep, cattle, goats and pigs are intermediate hosts

Severe clinical syndrome, cystic hydatid disease

Education of food handlers and consumers regarding food preparation and personal hygiene. Echinococcus eggs are not susceptible to freezing (except when core temperature of food is minus 80°C for 48 hrs or minus 70°C for 4 days). E ective inspection system to ensure GHP and GAP. Ability to trace back to farm. Keeping dogs away from potentially infected o al and from near abattoirs. Echinococcus eggs are not susceptible to freezing (except when core temperature of food is minus 80°C for 48 hrs or minus 70°C for 4 days).

WHO/OIE, 2001. OIE, 2005a. WHO, 2011.

28 Severity of illness Examples of management options and challenges along the food Overarching chain factors for consideration in Post-harvest or Retail and risk management On-farm processing consumer Far more challenging to control than E. granulosus given the predominance of a sylvatic cycle involving foxes and rodents. Di cult to control in wildlife. Anthelminthic impregnated bait for foxes in peri-urban areas or around farms – may be di cult to sustain and also expensive. Echinococcus eggs are not susceptible to freezing Education of food handlers and consumers may be the most feasible form of control in endemic areas. Washing produce not be su cient to remove parasites. Echinococcus eggs not susceptible to freezing (see above). Education of high-risk consumer groups is imperative; this includes pregnant women and immunocompromised individuals. Commercial freezers can kill tissue cysts in meat; domestic freezers or cooling under gas or vacuum may not be e ective. Susceptible to pasteurization and cooking. Testing of meat & organ products not a viable option as cysts are small and randomly distributed. Lack of standardized methods means that fresh produce is not routinely tested for T. gondii oocysts. Challenging to control because there are multiple possible vehicles. Non-food-borne infections complicated by the domestic “house” cat as a known parasite reservoir and source of infection. Control feasible in housed or feedlot pigs and cattle (can be con rmed by serological testing - Toxoplasma-free designation) Not feasible in free range farmed animals. Vaccine available for sheep, but tissue cysts still present in meat. WHO/OIE, 2001. OIE, 2005a. WHO, 2011. Examples of risk management texts and guidance Severe clinical syndrome, alveolar echinococcosis Mild to moderate to severe, can cause abortions and congenital defects. May be linked to chronic mental and neurologic sequelae in adults. Jones and Dubey, 2012. Kijlstra and Jongert, 2008.

Parasite

Hosts and main transmission routes – Food chains of concern

Echinococcus multilocularis

Fresh produce. New trend may be migration of the parasites with sylvatic incursion into residential areas.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Toxoplasma gondii

Meat and o al from a range of animals (pigs, cattle, sheep, goats, game) may contain infectious tachyzoites. Oocysts can contaminate fresh produce and molluscan shell sh. Oocysts can be a source of on-farm infection for domestic animals.

Parasite

Hosts and main transmission routes – Food chains of concern Severity of illness Mild to moderate to severe and chronic (immuno compromised) Control measures for water quality throughout the water supply and food chain. Oocysts: (a) very resistant to chlorine, (b) detection methods do not assess viability, (c) can survive within, and be protected by, the stoma of fresh fruits and leafy vegetables. Composting may be insu cient to inactivate oocysts. No housing of calves (and other livestock) in areas where produce is grown. Thorough washing of farm equipment, e.g. collection baskets. Dedicated use of equipment may help control. Commercial tanks for washing produce can become contaminated. Transport vehicles, storage equipment & rooms important sources of crosscontamination. Susceptible to pasteurization and freezing. ISO developing a standard for detection in food. but expensive, e ciency may be low, small sample size may not account for heterogeneous distribution. Consumer education is critical for HIV+ and other immunocompromised individuals, at risk for severe and chronic infections. Fresh produce may be high risk. Washing of fresh fruits and vegetables recommended but will not remove all oocysts.

Examples of management options and challenges along the food Overarching chain factors for consideration in Post-harvest or Retail and risk management On-farm processing consumer ISO Standards. US-EPA Standards. UK-DWI Standards. Robertson and Fayer, 2012.

Examples of risk management texts and guidance

Cryptosporidium spp.

Fresh produce, fruit juice, and milk. Likely entry into the food chain is by water and/or contamination by food handlers. The entire water system must be addressed, e.g. reservoir, piping, etc.

CHAPTER 4 RISK MANAGEMENT OPTIONS FOR THE HIGHER RANKED PARASITE

Entamoeba histolytica

Fresh produce. Largely water-borne and associated with food handlers. The cysts are sensitive to chlorine washes.

Mild to moderately severe. Diarrhoeal illness, liver abscess.

Diagnosis of E. histolytica requires speci c tools to di erentiate it from non-pathogenic E. dispar and E. moshkovskii.

Theel and Pritt, Illnesses in the 2012 past have been linked to lack of hygiene during food preparation and consumption.

30 Severity of illness Examples of management options and challenges along the food Overarching chain factors for consideration in Post-harvest or Retail and risk management On-farm processing consumer Trichinellosis There are speci c occurs worldwide. recommendations for Trichinella-free pig farming and national herd certi cation programmes. Processing such as sausage making can spread one infected animal among many products, increasing the risk from a single contaminated animal. Examples of risk management texts and guidance Acute illness, low fatality rate FAO/WHO/OIE Controlled in 2007. many countries, OIE, 2005b where present, by consumer education to cook pork thoroughly. Controlled by some religious and ethnic dietary restrictions. During food preparation and consumption, Opisthorchiidae can be controlled by freezing and by thorough cooking. FAO, 2012 Severe infections, chronic sequelae, carcinogenic potential It may be impossible to control the infection in wild-caught sh. Currently, of regional importance for Asia. Discourage the feeding of unsterilized night soil (i.e. human faeces) to commercially farmed sh. Architecture and location of commercial ponds important to avoid contamination by faecal run-o .

Parasite

Hosts and main transmission routes – Food chains of concern

Trichinella spiralis

Pork, horse and game meat.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Opisthorchiidae

Freshwater sh. The parasite occurs in sh in the wild and very rarely in those grown under commercial aquaculture. Multiple hosts, e.g. farm animals.

TABLE 5. Commodity-trade volumes and monetary values of the primary food vehicles of transmission of the higher ranked parasites Food Category Beef and veal Pork Goat meat Sheep meat Game/wild animal meat Marine sh (edible product) Freshwater sh (edible product) Freshwater crustaceans (edible product) Marine crustaceans (edible product) Molluscan shell sh (bivalves) (edible product) Berries Fruit juice Other fruits Vegetables, fresh Trade volume (tonne) 2010 or 2009 (1) 5 208 618 3 728 741 53 431 962 169 55 198 22 431 962 3 627 385 31 818 2 947 344 466 790 123 417 2 707 796 1 955 370 2 444 437 Trade value (1000 US$) 2010 or 2009 (1) 23 893 619 10 061 812 239 167 5 110 599 477 096 49 163 711 17 797 345 226 837 19 591 627 2 148 135 571 570 3 527 824 1 660970 3 251 556

Sources: The information is based on that available for the year 2010 in the FAO Statistical database (FAOSTAT) as of 19 October 2012. (1) Information for sh, crustaceans and bivalves are for the year 2009, based on the latest available data from FAO Fisheries and Aquaculture Statistics Service, 2012.

CHAPTER 4 RISK MANAGEMENT OPTIONS FOR THE HIGHER RANKED PARASITE

5 Conclusions and recommendations Providing risk managers with the information they need for decision-making is

a critical element of food safety management. is meeting of technical experts was convened with the objective of providing information for globally important food-borne parasites. Given the breadth of the area of food-borne parasites, FAO and WHO concluded that addressing the task required a structured and transparent approach that made optimal use of existing information and was able to build on existing and relevant initiatives underway in both organizations. is led to the development of a multicriteria-based ranking tool, and challenged all the participants to use the available information and their expertise and apply it to the ranking exercise. While this initiative took substantial e ort, the meeting concluded that the output, a transparent, reproducible and qualitative (with quantitative inputs) approach to ranking food-borne parasitic hazards of global importance and the application of that tool to produce a global ranking of food-borne hazards of concern was signi cant, and should provide CCFH with the requested overview of the parasite-commodity combinations of concern. It is important to acknowledge that the present ranking is global and based on the state of knowledge and experience in 2012. Taking a global perspective, it is

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

not expected that this would necessarily re ect parasite ranking at national level, where more precise information may be available and speci c local conditions can be taken into consideration. For the current ranking, it is fully recognized that this could change as more research, data and information on food-borne parasites become available for further analysis and ranking re nement. Like many phases of risk analysis, this process is potentially most useful if it is replicated and updated on a continuous basis. Furthermore, it is well recognized that initiatives such as the FERG initiative to assess the global burden of food-borne disease will in the medium term provide much more extensive information in terms of the public health importance and burden of food-borne diseases and be critical to furthering our understanding and knowledge. However, like any in-depth study, they are also resource and time intensive. In the meantime, ranking approaches such as the one described here allow the use of whatever information is available at a particular point in time to identify those parasites (or other hazards) of greatest concern and also to take into account aspects other than the public health element. e systematic and transparent approach means that they can be updated as new information comes on board and can be considered as one means of translating existing knowledge on foodborne parasites into a format that focuses the risk manager’s attention. e meeting concluded that food-borne parasites had not always received the attention they deserved based on their public health, trade and socio-economic importance. It was hoped that exercises such as this would serve to increase the awareness of food-borne parasites at a global level. Although it was recognized that the current meeting was aimed at providing advice to the CCFH, managing foodborne parasites is clearly a multidisciplinary task with a critical role for partners, not only those working with di erent parts of the food chain, but also in diverse disciplines addressing water, wildlife, the environment and more. e meeting recognized that the ranking alone is not adequate for decisionmaking, and that the establishment of priorities by risk managers also requires consideration of other factors. erefore, the experts aimed to provide additional information which could facilitate the decision-making process, including the primary food vehicles of concern for each of the parasites, knowledge on food attribution, and some information in relation to control of these parasites. An example of how these di erent elements could then be used by risk managers is presented in Annex 6. However, this report does not profess to be fully comprehensive, but rather raises awareness of certain aspects to be considered in the preliminary risk management phase. e existing materials, particularly for management of zoonotic parasites at the primary production stage, were fully acknowledged, and the meeting highlighted the importance of updating such texts. For example, CHAPTER 5 CONCLUSIONS AND RECOMMENDATIONS

the meeting recommended that the FAO/WHO/OIE guidelines for the surveillance, prevention and control of trichinellosis (2007) be periodically reviewed and updated to re ect technological advances. e meeting also recognized that there are numerous knowledge gaps that hamper our e orts to control food-borne parasites, including the di culty of attributing food or other vehicles for the transmission of parasite infection and illness. e importance of ongoing research into food-borne transmission of parasites was emphasized. One example is where recent studies suggest that, for Toxoplasma gondii, oocyst infection attributed to produce might be much more important than previously thought. While it was not within the scope of this meeting to address such aspects in detail, the meeting did recommend that if Codex decides to move forward with development of risk management guidance for speci c parasites, then it should request more speci c scienti c input on the individual parasites.

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Muñoz-Zanzi, C.A., Fry, P., Lesina, B. & Hill, D. 2010. Toxoplasma gondii oocyst-specific antibodies and source of infection. Emerging Infectious Diseases, 16(10): 1591– 1593. Ng, V. & Sargeant, J.M. 2012. A stakeholder-informed approach to the identi cation of criteria for the prioritization of zoonoses in Canada. PLoS One, 7(1): e29752. [Online. doi: 10.1371/journal.pone.0029752.] OIE (World Organisation for Animal Health). 2005a. Terrestrial Animal Health Code, Chapter 8.4, Echinococcosis/Hydatidosis. See: http://www.oie.int/en/international-standard-setting/terrestrial-code/access-online/ Accessed 2013-07-06. Note that Chapter 8.4 is currently (July 2013) under revision, revising Chapter 8.4 for E. Granulosu, with a proposed new chapter for E. multilocularis. OIE. 2005b. Terrestrial Animal Health Code, Chapter 8.13, Trichinella spp. See:http:// www.oie.int/en/international-standard-setting/terrestrial-code/access-online/ Accessed 2013-07-06. Note that Chapter 8.13 is currently (July 2013) under revision. Orlandi, P.A., Chu, D.-M.T., Bier, J.W. & Jackson, G.J. 2002. Parasites and the food supply. Food Technology 56(4): 72–81. Polley, L. & ompson, R.C.A. 2009. Parasite zoonoses and climate change: molecular tools for tracking shi ing boundaries. Trends in Parasitology, 25(9): 285–291. Robertson, L.J. & Fayer, R. 2012. Cryptosporidium. pp. 33–64 (Chapter 2), in: L.J. Robertson and H.V. Smith (editors). Food-borne Protozoan Parasites. Nova Scotia Publishers, Inc., Hauppauge, NY, USA. Rohr, J.R., Dobson, A.P., Johnson, P.T.J., Kilpatrick, A.M., Paull, S.H., Ra el, T.R., Ruiz-Moreno, D.R. & omas, M,B. 2011. Frontiers in climate change – disease research. Trends in Ecology and Evolution, 26(6): 270–277. Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., Jones, J.L. & Gri n, P.M. 2011. Foodborne illness acquired in the United States – major pathogens. Emerging Infectious Diseases, 17(1): 7–15. Sli o, T.R., Smith, H.V. & Rose, J.B. 2000. Emerging parasite zoonoses associated with water and food. International Journal for Parasitology, 30: 1379–1393. eel, E. & Pritt, B.S. 2012. Balantidium coli and Entamoeba histolytica. pp. 2–32 (Chapter 1) in: L.J. Robertson and H.V. Smith (editors). Food-borne Protozoan Parasites. Nova Scotia Publishers, Inc., Hauppauge, NY, USA. WHO. 2011. Report of the WHO Informal Working Group on cystic and alveolar echinococcosis, surveillance, prevention and control, with the participation of FAO and OIE. 22–23 June, 2011. Department of Control of Neglected Tropical Diseases, WHO, Geneva, Switzerland. 20 p. Available at www.who.int/entity/neglected_diseases/diseases/echinococcosis/en/ Accessed 2013-07-04.

REFERENCES

WHO/FAO/OIE. 2005. Guidelines for the surveillance, management, prevention and control of taeniosis/cysticercosis. Edited by K.D. Murrell and seven others. 99 p. Available at http://www.oie.int/doc/ged/d11245.pdf Accessed 2013-07-05. WHO/OIE. 2001. WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. Edited by J. Eckert, M.A. Gemmell, F.-X. Meslin and Z.S. Pawlowski. 285 p. Available at http://whqlibdoc.who.int/ publications/2001/929044522X.pdf Accessed 2013-07-05.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Annexes

Annex 1 Identi cation of food-borne parasites for consideration An online questionnaire was utilized to prioritize 93 listed parasites at a regional and global level with respect to their public health signi cance and trade implications. e questionnaire also provided a valuable resource for the experts in developing criteria to be used for the ranking process (Table A1.1). e results were grouped into four tiers related to the global relevance of the listed parasites. Tier 1 and Tier 2 parasites were classi ed as “important” (‘very’ or ‘somewhat’) from a global perspective by at least 50% (n=25) and 40% (n=12) of experts, respectively.

TABLE A1.1 Tiered list of parasites under consideration Tier 1 parasites (identi ed by more than 50% of the experts as being globally important) Anisakis simplex Anisakis spp. Ascaris lumbricoides Clonorchis sinensis Cryptosporidium hominis. Cryptosporidium parvum Cryptosporidium spp. Diphyllobothrium latum Diphyllobothrium spp. Tier 2 parasites (scored by more than 40% of experts as being globally important) Ancylostoma duodenale Balantidium coli Cyclospora cayetanensis Enterobius vermicularis Gnathostoma spinigerum Hymenolepis nana Metagonimus spp. Necator americanus Opisthorchis felineus Sarcocystis spp. Taenia asiatica Trichinella nativa Echinococcus granulosus Echinococcus multilocularis Entamoeba histolytica Fasciola gigantica Fasciola hepatica Giardia lamblia Taenia saginata Taenia solium Toxocara canis Toxocara cati Toxoplasma gondii Trichinella britovi Trichinella pseudospiralis Trichinella spiralis Trichuris trichiura Trypanosoma cruzi

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Tier 3 parasites (those with the greatest number of “very important” global scores or regional scores and those with the highest cumulative importance scores, i.e. sum of number of experts indicating a parasite is global and regionally important) Angiostrongylus cantonensis Blastocystis spp. Capillaria philippinensis Fasciolopsis buski Tier 4 – Remaining parasites Alaria alata Alaria americana Alaria spp. Ancylostoma ceylanicum Echinostoma revolutum Echinostoma spp. Gastrodiscoides hominis Gnathostoma binucleatum Nanophyetus salmincola Paragonimus kellicoti Pseudoterranova decipiens Sarcocystis fayeri Sarcocystis suihominis Spirometra erinacei Spirometra mansoni Spirometra mansonoides Spirometra ranarum Spirometra spp. Taenia multiceps Taenia serialis Trichinella papuae Trichinella zimbabwensis Trichostrongylus spp. Opisthorchis viverrini Paragonimus heterotremus Paragonimus spp. Paragonimus westermani Sarcocystis hominis Strongyloides stercolaris Trichinella murelli

Angiostrongylus costaricensis Gnathostoma hispidu Baylisascaris Blastocystis hominis Capillaria hepatica Centrocestus spp. Contracaecum/Phocascaris Cystoisospora belli Dicrocoelium dendriticum Dientamoeba fragilis Dioctophyme renale Diplogonoporus grandis Haplorchis pumilo Haplorchis spp. Haplorchis taichui Heterophyes spp. Hymenolepis diminuta Kudoa septempunctata Lecithodendriid ukes Linguatula serrata Mesocestoides lineatus Mesocestoides variabilis

e Tier 3 list comprised those with the greatest number of “very important” global scores or regional scores, and those with the highest cumulative importance scores (sum of number of experts indicating a parasite is global or regionally important ), while Tier 4 contained the remaining parasites. e experts decided to further screen this 4-tiered list through grouping of parasites by genus or family (Table A1.2), and where applicable, based on common routes of transmission, clinical manifestations, and food-borne sources of infection. is resulted in a list of 24 parasites for the ranking exercise (Table 2 in Section 2.2 in the main report). Table A1.3 lists parasites that were considered important by the experts at the regional or national level but were excluded at the global level for the stated reasons. CHAPTER 1 INTRODUCTION

TABLE A1.2. Parasite groupings

Parasites Anisakis simplex Anisakis spp. Pseudoterranova decipiens

Grouping Anisakidae

Parasite Paragonimus heterotremus Paragonimus spp. Paragonimus westermani Paragonimus kellicoti Sarcocystis spp. Sarcocystis hominis Sarcocystis fayeri Sarcocystis suihominis Spirometra erinacei Spirometra mansoni Spirometra mansonoides Spirometra ranarum Spirometra spp. Toxocara canis Trichinella britovi Trichinella pseudospiralis Trichinella native Trichinella murelli Trichinella papuae Trichinella zimbabwensis

Grouping Paragonimus spp.

Cryptosporidium hominis Cryptosporidium parvum Cryptosporidium spp. Diphyllobothrium latum Diphyllobothrium spp. Diplogonoporus grandis

Cryptosporidium spp.

Sarcocystis spp.

Diphyllobothriidae

Spirometra spp.

Fasciola gigantica Fasciola hepatica Metagonimus spp. Centrocestus spp. Heterophyes spp. Haplorchis pumilo Haplorchis spp. Haplorchis taichui

Fasciola spp. Heterophyidae

Toxocara spp. Trichinella spp.

Opisthorchis felineus Opisthorchis viverrini

Opisthorchiidae

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

TABLE A1.3. Parasites excluded from original list Broad Category Parasites EXCLUDED Criteria for exclusion

Meat-borne

Taenia asiatica Taenia serialis

Regional Unlikely / rare zoonosis Regional – Philippines Proportion of cases attributable to food-borne infection negligible Regional – SE Asia Regional – SE Asia Regional – SE Asia Regional – SE Asia Proportion of cases attributable to food-borne infection negligible Proportion of cases attributable to food-borne infection negligible Proportion of cases attributable to food-borne infection negligible Proportion of cases attributable to food-borne infection negligible Regional – Asia Paci c Proportion of cases attributable to food-borne infection negligible

Fish- and shell shborne

Capillaria philippinensis Contracaecum/ Phocascaris Echinostoma spp. Gnathostoma spp. Kudoa septempunctata Lecithodendrid ukes

Plant (fruit- and vegetable-borne, including berries, fruit juice)

Blastocystis spp. Strongyloides stercoralis Ancylostoma spp. Necator americanus

“Other”

Angiostrongylus cantonensis Hymenolepis spp.

CHAPTER 1 INTRODUCTION

Annex 2 Food-borne parasite ranking exercise: summary card Group: Criterion Number of global food-borne illnesses (manifesting disease) Global distribution (number of regions) Acute morbidity severity (disability weight) Chronic morbidity severity (disability weight) Fraction of illness that is chronic (%) Case-fatality ratio (%) Likelihood of increased human burden (%) How relevant is this parasite-food pathway for international trade? Scope of impact to economically vulnerable communities? Bin 0 Parasite/food: Bin 1 10 000 – 100 000 Bin 2 100 000 – 1 000 000 Bin 3 1 000 000 – 10 000 000 Bin 4 Score

<10 000

>107

N/A

1 <0.03 (very mild) <0.03 (very mild) <25% chronic 0–0.1% 0–25% (low)

2 0.03–0.1 (mild) 0.03-0.1 (mild) 25–50% chronic 0.1–1% 25–50% (moderate)

3-4 0.1–0.30 (moderate) 0.1–0.30 (moderate) 50–75% chronic 1–10% 75–100% (high)

>4 >0.30 (severe) >0.30 (severe) >75% chronic >10% 100% (still increasing)

0 (none)

0%chronic

None

Not at all

Some relevance

High relevance

None

Low

Moderate

High

What is the quality of available evidence Very Poor for this parasite?

Poor

Adequate

Good

Very Good

Further comments relevant for the discussion on risk management

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Annex 3 Food-borne parasite ranking exercise form: explanation of criteria e summary card used to conduct this exercise should be considered an expert elicitation. We are asking for your expert judgment on 9 scored parameters, each of which is intended to capture some aspect of the global importance of each parasite. We realize that data may not be available to support your scores, but we ask you to use your knowledge of the literature and your considered opinion to answer these questions. Please indicate group and parasite/food pathway on the sheet. We ask that for each parasite you estimate each criterion, using the levels marked in the bins to indicate your group score. You may circle multiple bins as marked in the example below to indicate a broader range of values, but it is CRITICAL that you come to a SINGLE CONSENSUS BEST GUESS SCORE for the criterion and mark it numerically in the rightmost column. Please take notes on a separate piece of paper to indicate important assumptions or data sources that you would like to record. Please mark on that paper the group and parasite/food pathway so we can associate it with your scores. Please remark additional comments relevant to risk management below and on the back. Example: Bin 0 Mortality rate (case-fatality ratio) (%) Bin 1 Bin 2 Bin 3 Bin 4 Score

0–0.1%

0.1–1%

1–10%

>10%

Criterion No. 1. Number of global food-borne illnesses Criterion: Explanation: Number of individuals worldwide that manifest clinical illness is criterion measures the magnitude of global food-borne disease as the number of people worldwide who have clinical

ANNEX 3

FOOD BORNE PARASITE RANKING EXERCISE FORM: EXPLANATION OF CRITERIA

symptoms of illness and who were infected by food. If you do not feel that you can estimate this number directly, you can calculate it based on numbers you may feel more comfortable with. Namely, it can be considered a function of the global prevalence of infection multiplied by the percent of infections that are result from food consumption multiplied by the percent of infections that are symptomatic multiplied by the global population of (7 billion people). For parasites that are generally regarded as acute infections (e.g. Trichinella), it is incidence times percent symptomatic times percent food-borne times global population. For example: Your best estimate is that Parasite A has a global prevalence of about 20%, of which about 50% you believe to be food-borne. Of these infections, the literature suggests that 10% of infections are symptomatic. is equates to a global illness rate of 1% (20% × 50% × 10%). us, you would estimate about 70 000 000 cases (1% of 7×109).

Ranges: Bin 0 Bin 1 Bin 2 Bin 3 Bin 4

<10 000 10 000 – 100 000 100 000 – 1 000 000 1 000 000 – 10 000 000 >10 000 000 illnesses illnesses illnesses illnesses illnesses

Criterion No. 2. Geographical distribution (endemic regions) Criterion: Number of regions in which this parasite is geographically distributed (in which it shows a natural cycle) is criterion re ects the global distribution of the parasite across world regions as a simple count of the number of major regions (Africa, Asia, Europe, Near East, North America, Latin America and the Carribbean, Paci c) in which the disease is regularly found.

Explanation:

Ranges: Bin 0 Not applicable Bin 1 1 region Bin 2 2 regions Bin 3 3-4 regions Bin 4 > 4 regions

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Criterion No. 3. Acute Morbidity Severity Criterion: Explanation: Loss of health-related quality of life due to acute infection is criterion re ects the degree to which an acute manifestation of illness reduces health-related quality of life. e value of the criterion is anchored between 0 (full health, asymptomatic, no illness) to 1 (worst possible health state or death). It depends on both the severity and duration of illness. For a large number of health conditions, including many infectious diseases and some parasitic diseases, disability weights have already been published.

Ranges: Bin 0 0 (none) Bin 1 < 0.03 (very mild) Bin 2 0.03 –0.01 (mild) Bin 3 0.01–0.30 (moderate) Bin 4 >0.30 (severe)

Decision rules: If a pathogen causes more than one acute disease, a population weighted average is applied. Calculate your best guess point estimates for identi ed acute conditions and weight by likelihood. en assign a bin using the ranges above. Refer to the table of disability weights below (from Havelaar et al., 2010; Annex 1) or see WHO publications. e Global Burden of Disease 2004 Update includes a summary table on page 33 (WHO, 2008). is annex to the 2004 report includes more detailed disability weights (WHO, 2004; see http://www.who.int/healthinfo/global_burden_disease/GBD2004_DisabilityWeights.pdf) Table of disability weights for acute and chronic conditions Very mild (disability weight <0.03) Otitis media Hepatitis Folliculitis Cystitis Gastroenteritis, severe Duration (in days) 14 30 7 14 10–15 Moderate (0.1<disability weight <0.3) In ammatory bowel disorder Reactive arthritis Tuberculosis Chronic pulmonary disease (bronchitis, asthma, emphysema) Duration (in days) 183 183 365 365

ANNEX 3

FOOD BORNE PARASITE RANKING EXERCISE FORM: EXPLANATION OF CRITERIA

Conjunctivitis Tonsillitis Bronchitis Mild (0.03<disability weight <0.1) Allergic rhinitis Reactive arthritis Tinea pedis Eczema Otitis externa Gastroenteritis, hospitalized Laryngitis Sinusitis Irritable bowel syndrome Haemolytic uremic syndrome Visual disorder, mild Hepatitis Gastroenteritis, chronic In uenza

7 7 14

Diabetes mellitus

365

High (disability weight >0.3) 119 42 183 35 35 7–14 7 183 183 30 365 92 183 14 Renal failure Guillain-Barré syndrome Visual disorder, severe Paraplegia AIDS Meningitis Dementia 365 365 365 365 365 365

Criterion No. 4. Chronic Morbidity Severity Criterion: Loss of health-related quality of life associated with chronic illness. is criterion re ects the degree to which a chronic manifestation of illness reduces health-related quality of life. e value of the criterion is anchored between 0 (full health, asymptomatic, no illness) to 1 (worst possible health state or death). It depends on both the severity and duration of illness. For a large number of health conditions, including many infectious diseases and some parasitic diseases, disability weights have already been published.

Explanation:

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Ranges: Bin 0 0 (none) Bin 1 <0.03 (very mild) Bin 2 0.03–0.01 (mild) Bin 3 0.01–0.30 (moderate) Bin 4 >0.30 (severe)

Decision rules:

If a pathogen causes more than one chronic disease, a population weighted average is applied. Calculate your best guess point estimates for identi ed chronic conditions and weight by likelihood. en assign a bin using the ranges above.

Refer to Criterion 3 for additional guidance on disability weights.

Criterion No. 5. Fraction chronic Criterion: Percent of global food-borne illnesses (estimated in Criterion 1) that are considered chronic (see note below; this is a weighting criterion only) is criterion is used to partition the illnesses estimated in Criterion 1 into those with acute manifestations and those with chronic manifestations (scored in Criteria 3 & 4). It is assumed that 100% of illnesses estimated in Criterion 1 manifest in either acute or chronic illness. Note that this fraction will not be directly scored as a criterion in the scoring model; rather, it will be used to weight acute and chronic disease severities (Criteria 3 & 4). erefore, the bin numbers do not go from “less important” to “more important” as do categories for other parasites.

Explanation:

Ranges: Bin 0 Bin 1 Bin 2 Bin 3 Bin 4

<25% chronic

25–50% chronic

50–75% chronic

>75% chronic

Decision rule:

We recognize that some portion of chronic illness may be preceded by acute infection and therefore the actual percentages may not add up to 100%. However, for this exercise, we ask you to ignore this overlap and simply focus on providing a best estimate for the fraction that is chronic.

ANNEX 3

FOOD BORNE PARASITE RANKING EXERCISE FORM: EXPLANATION OF CRITERIA

Criterion No. 6. Mortality rate Criterion: Explanation: Case-fatality ratio is criterion estimates the likelihood that a given cases of illness will result in death. Mortality rate is dependent on disease symptoms and severity, as well as underlying health of the infected person.

Ranges: Bin 0 0% Bin 1 0 –0.1% Bin 2 0.1–1% Bin 3 1–10% Bin 4 >10%

Criterion No. 7. Increasing trend in disease Criterion: Explanation: Likelihood of a signi cant increase in human illness. is criterion re ects the potential for the human health burden associated with this particular parasite to increase in the near term, for example through changes in food production, processing and consumption.

Ranges: Bin 0 None Bin 1 0–25% (low) Bin 2 25–50% (moderate, or unsure) Bin 3 75–100% (high) Bin 4 100% (still increasing)

Criterion No. 8. International trade Criterion: Relevance of the parasite and its PRIMARY food sources or vehicles to a ect international trade. is qualitative criterion estimates the degree to which this particular parasite and its main food sources or vehicles may a ect international trade. While the characteristics of the parasite or disease severity relate to trade, it is largely a function of the food source or vehicle; if the primary food-borne pathway is not widely traded, or not currently traded from a region in which the parasite is currently endemic, it may not be likely to have an impact on trade. At the same time, if the parasite is in a food product that is widely traded or if there are current issues associated with the parasite-food pathway, it is of greater relevance.

Explanation:

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Ranges: Bin 0 No relevance Bin 1 Some relevance Bin 2 High relevance

Criterion No. 9. Distributional impacts (socio-economic impact)

Criterion: Explanation:

Scope of impact to economically vulnerable populations is criterion re ects the degree to which this disease a ects economically vulnerable communities, namely the extent to which this parasite causes reductions in household or community productivity, or the ability of a household or community to have access food (i.e. can produce and/or purchase food). Vulnerable communities include pastoral communities, small shing communities, small rural communities in developing countries, migrant populations in developed countries, minority indigenous populations (Inuit in Canada, aboriginals in Australia), or other similar communities.

Ranges: Bin 0 None Bin 1 Low Primarily a ects individual households; a ected households have reduced productive capacity or have reduced access to food Bin 2 Moderate Primarily impacts individual households but also a ects communities; households have reduced productive capacity or access to food; communities also have some reduced productive capacity or access to food Bin 3 High A ects entire communities; communities bear major losses to productive capacity and/or have seriously diminished access to food.

ANNEX 3

FOOD BORNE PARASITE RANKING EXERCISE FORM: EXPLANATION OF CRITERIA

Criterion No. 10. Quality of evidence Criterion: Quality of available evidence to support judgments (Not a scored criterion) is question re ects the extent to which you feel you were able to assess criterion-based data or information for a speci c parasite.

Explanation:

Ranges: Bin 0 Very Poor Bin 1 Poor Bin 2 Adequate Bin 3 Good Bin 4 Very Good

Comments Lastly, please indicate comments, if any, that should be considered in the discussion of risk management for this parasite food pathway

References Havelaar, A.H., van Rosse, F., Bucura, C., Toetenel, M.A., Haagsma, J.A., Kurowicka, D., Heesterbeek, J.H., Speybroeck, N., Langelaar, M.F., van der Giessen, J.W., Cooke, R.M. & Braks, M.A. 2010. Prioritizing emerging zoonoses in the Netherlands. PLoS One, 5(11): e13965. [Online doi: 10.1371/journal.pone.0013965.] WHO. 2004. Global burden of disease 2004 update: Disability weights for diseases and conditions. Available at http://www.who.int/healthinfo/global_burden_disease/ GBD2004_DisabilityWeights.pdf Accessed 2013-07-05. WHO. 2008. Global Burden of Disease 2004 Update. See http://www.who.int/healthinfo/ global_burden_disease/GBD_report_2004update_part3.pdf Accessed 2013-07-05.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Annex 4 Criteria weights worksheet e overall parasite score is given by two equations: C1*W1 + C2*W2 + C345*W345 + C6*W6 + C7*W7 + C8*W8 + C9*W9 Eq. 1 C345={C3*(1-C5) + C4*C5} Eq. 2 where C are criteria scores normalized to a 0–1 scale and W are the criteria weights, which sum to 100%. Eq. 2 calculates the average severity weight for the parasite, an average of chronic disability weight and acute disability weight using the fraction of illnesses that are chronic. us, criteria 3, 4 and 5 have one associated weight, denoted as W345. Otherwise the calculation is straightforward: normalized parasite criteria scores are multiplied by fractional weights. Criteria weights are simply the fraction of the total score re ected by the criteria in question. erefore, if you think 25% of the overall score should be driven by C1, W1 should be marked with a 25. For comparison purposes, equal weighting of all criteria would result in a value of 14.285%. Make sure that all numbers sum to 100%, and that no criterion weight is less than 5%. Please use integers only (no decimal points). Criterion C1. Number of global food-borne illnesses C2. Global distribution C3. Acute morbidity severity C4. Chronic morbidity severity C5. Chronic illness fraction C6. Case fatality rate C7. Increasing illness potential C8. Trade relevance C9. Impacts to economically vulnerable communities SUM Weighting Code W1 W2 Criterion Weight (Fraction of Total Score)

W345

W6 W7 W8 W9 100%

ANNEX 4 CRITERIA WEIGHTS WORKSHEET

Annex 5 Sensitivity analysis In addition to the results presented in the main text, a number of analyses were conducted to examine elicited scores and the sensitivity of the ranking results to di erent model inputs. First, variability was examined across groups in elicited scores. Figure A5.1 shows group scores for all nine criteria, averaged over all parasites scored by each group. Because each group scored a slightly di erent set of parasites, the average scores are not directly comparable, but they do show some interesting patterns. Criterion 2, on the global distribution of disease of each parasite, shows consisScaled Criteria Scores (0-1) 0.0 1. Number of illnesses 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0

2. Global distribution

3. Acute Severity

4. Chronic Severity

5. Fraction Chronic

6. Case Fatality Rate

7. Illness trends

8. Trade revlevancy 9. Vulnerable communities

Group 1 Group 2 Group 3 Group 4 Group 5

FIGURE A5.1. Group scores by criteria, averaged across parasites

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

tently high average scores, which suggests that experts generally agreed that the set of screened pathogens re ects parasites of global relevancy. e severity of chronic disease consistently scored higher than the severity of acute disease for this set of parasites. Overall, scores for illness trends were low, suggesting that current, endemic disease may be more of a concern than disease movement or emergence.

Average criterion score (0-2)

FIGURE A5.2. Means and ranges of normalized risk scores across expert groups under baseline model conditions

ANNEX 5 SENSITIVITY ANALYSIS

Just as there is variability across expert groups in average criteria scores across parasites, there is variability across groups for speci c parasites. is is shown in Figure A5.2, which shows the mean normalized risk scores presented in the main text of the report, as well as the ranges of estimates across groups. Some parasites, such as Toxoplasma gondii, have relatively little variability across experts, while parasites such as Echinococcus multilocularis and Paragonimus, have notably larger variability. is variance can be interpreted as a signal of the strength of scienti c knowledge about a given parasite: the greater the variance, the greater the uncertainty in information available to experts. In examining sensitivity of the model itself, alternative weighting schemes were of particular interest. In some multi-criteria decision analyses, di erent groups of experts are used to score the individual criteria and to develop the weights that de ne how criteria scores will be combined into a nal risk score. at is, subject matter experts are elicited for criteria scores, while risk managers are elicited for criteria weights. In part due to time and resource constraints, weights were elicited from expert groups, as well as from the FAO/WHO Secretariat, acting as risk managers. e mean of elicited weights across all participants was used for the baseline model and ranking. Criterion weights were roughly similar across experts and risk managers, as shown in the rounded values presented in Table A5.1. Risk managers tended to put greater weight on potential for increased illness, trade relevance and impacts to economically vulnerable communities than did experts, but all participants tended to put greater weight on public health criteria. ese are compared with an equal weighting scheme, in which each criterion is treated as of equal importance in the overall risk score. Sensitivity analyses of rankings were conducted around three alternative weighting schemes: mean of expert weights, mean of risk manager weights, and equal criteria weighting. Table A5.2 and Figure A5.3 show multicriteria risk scores (normalized to 0–100) for global foodborne parasites for the baseline and the three alternative schemes mentioned above. Although di erent schemes result in slightly di erent scores, the ranking is fairly robust among the alternative schemes. Sensitivity analyses of rankings were conducted around three alternative weighting schemes: mean of expert weights, mean of risk manager weights, and equal criteria weighting. Table A5.2 and Figure A5.3 show multicriteria risk scores (normalized to 0–100) for global foodborne parasites for the baseline and the three alternative schemes mentioned above. Although di erent schemes result in slightly di erent scores, the ranking is fairly robust among the alternative schemes. 56 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

TABLE A5.1. Mean of elicited criteria weights used in multicriteria ranking Weighting Scoring criterion Baseline W1. Number of global foodborne illnesses Global distribution 0.22 Expert 0.24 Secretariat 0.20 Equal 0.14

W2.

0.14 0.22 0.15 0.07 0.10 0.10

0.15 0.23 0.16 0.06 0.06 0.09

0.12 0.21 0.15 0.09 0.13 0.11

0.14 0.14 0.14 0.14 0.14 0.14

W345. Morbidity severity W6. W7. W8. W9. Case-fatality ratio Increasing illness potential Trade relevance Impacts on economically vulnerable communities

Given the similarities in expert and Secretariat scores, the biggest di erences can be seen in the equal weighting scheme, though even under that scheme the ranks of the rst four parasites are identical. Figure A5.4 shows how these alternativee schemes a ect the rank order of parasites in the overall ranking. e dots show the baseline rank, while the vertical lines display the range of ranks across the three alternative scenarios. is gure shows that ranks are quite stable, with some parasite-speci c deviation. ose with the greatest deviation in scores are Taenia saginata and Cyclospora cayetanensis, followed by Trichinella spiralis, Ascaris spp., Paragonimus spp., Anisakidae and Toxocara spp. Most of these are parasites with higher scores in trade relevancy or impacts on socio-economically vulnerable populations, as the equal weighting scheme increases the importance of these criteria. TABLE A5.2. Normalized multicriteria risk scores for global foodborne parasites under alternative criteria weighting schemes Weighting scheme Baseline Taenia solium Echinococcus granulosus Echinococcus multilocularis Toxoplasma gondii 72.9 63.6 61.6 61.0 Expert 73.1 65.9 65.0 64.9 Secretariat 72.7 61.8 58.8 57.7 Equal 70.7 60.5 56.8 53.0

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Cryptosporidium spp. Entamoeba histolytica Trichinella spiralis Opisthorchiidae Ascaris spp. Trypanosoma cruzi Giardia duodenalis Fasciola spp. Cyclospora cayetanensis Paragonimus spp. Trichuris trichiura Trichinella spp.* Anisakidae Balantidium coli Taenia saginata Toxocara spp. Sarcocystis spp. Heterophyidae Diphyllobothriidae Spirometra spp.

51.8 51.8 49.9 47.9 47.1 45.4 44.7 42.7 40.6 39.5 36.6 36.0 34.1 33.0 32.3 30.8 30.3 29.3 25.2 22.5

54.7 55.5 48.8 49.3 50.9 46.6 48.0 44.5 40.4 41.9 39.6 36.6 33.1 35.6 30.7 33.7 31.1 30.2 25.9 23.5

49.4 48.7 50.8 46.7 43.9 44.4 41.9 41.3 40.8 37.5 34.0 35.5 35.0 30.8 33.7 28.4 29.7 28.5 24.7 21.6

46.9 46.0 50.1 43.8 40.1 40.1 38.5 39.8 41.6 34.2 32.1 36.4 36.1 29.7 35.6 26.2 29.4 27.8 24.3 19.8

In addition to examining alternative criterion weights, alternative sets of criteria were explored. In particular, rankings were generated based on public health criteria alone. Figure A5.3 shows the result of an alternative ranking model utilizing only criteria 1–6, with equal criteria weighting (W1=W2=W345=W6=0.25). ese results show greater di erences than with prior exploration of weighting schemes alone, though the order is largely preserved. e removal of the other criteria resulted in a notable downward shi in rankings of parasites with trade importance, such as Taenia solium, Trichinella spiralis, Taenia saginata, Cyclospora spp. and Anisakidae. is sensitivity analysis suggests that while trade relevancy is not the primary driver underlying overall risk scores in the baseline scenario, it did exert an important in uence on the nal rankings.

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Taenia solium Echinococcus granulosus Echinococcus multilocularis Toxoplasma gondii Cryptosporidium spp. Entamoeba histolytica Trichinella spiralis Opisthorchiidae Ascaris spp. Trypanosoma cruzi Giardia duodenalis Fasciola spp. Cyclospora cayetanensis Paragonimus spp. Trichuris trichiura Trichinella spp.* Anisakidae Balantidium coli Taenia saginata Toxocara spp. Sarcocystis spp. Heterophyidae Diphyllobothriidae Spirometra spp. 0 10 20 30 40 50 60 70 80 Baseline weights Expert weights Secretariat weights Equal weights

FIGURE A5.3. Comparison of multicriteria risk scores of global foodborne parasites across alternative criterion weighting schemes

Normalized overall score

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FIGURE A5.4. Rank scores of global foodborne parasites across alternative criterion weighting schemes, presented as ranges around baseline ranks

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Echinococcus multilocularis Toxoplasma gondii Taenia solium Echinococcus granulosus Entamoeba histolytica Cryptosporidium spp. Ascaris spp. Giardia duodenalis Trichinella spiralis Opisthorchiidae Trypanosoma cruzi Fasciola spp. Paragonimus spp. Trichuris trichiura Balantidium coli Toxocara spp. Trichinella spp.* Anisakidae Cyclospora cayetanensis Sarcocystis spp. Heterophyidae Taenia saginata Diphyllobothriidae Spirometra spp. 0 10 20 30 40 50 60 70 80 Public health criteria only, equal weights All criteria, baseline weights

Normalized overall score

FIGURE A5.5. Multicriteria ranking of global foodborne parasites based on public health criteria only, weighted equally, compared with baseline ranking based on all criteria and elicited weightingsc

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Annex 6 Risk management actions e Codex Alimentarius Commission recognizes the requirement for a multidisciplinary inter-sectoral approach for the control of food-borne parasites, given their unique life-cycles and epidemiology as demonstrated by their e orts to work closely with OIE as well as FAO and WHO in the development of risk management guidance related to speci c parasites. However, as Codex is aiming to address food-borne parasites in a more generic manner, as well as to develop speci c guidance for priority hazards, following the trend towards risk-based standards and adopting a food-chain approach, Codex requested additional information from FAO and WHO to assist it in that endeavour. is report aims to provide at least some of the information required by CCFH in prioritizing its work on food-borne parasites. An example of a decision-tree approach that CCFH or other risk managers could use in the prioritization of ranked parasites and their primary vehicle of concern is presented below. FIGURE A6.1. Decision tree for the risk management process Are there non-health considerations introduced by the risk manager which may lead to prioritization? Separate risk management process No

Q1. Rank

Is the parasite / food a high rank? Yes Does the global health burden have a signi cant proportion associated with a food commodity that has a high global volume? Yes CCFH Are control measures available that will reduce the health burden cf. the current (ranked) situation? Yes (If in Codex jurisdiction)

Q2. Global vs trade importance

Stop

Stop (inform other agencies? E.g. WHO, FAO)

Q3. Availability of control measures

Stop

Q4. Type of standard required

Is general or speci c guidance on parasite control needed?

CCFH prioritise the work needed (include review of existing standards)

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Annex 7 Speci c information for the ranked parasites For a Glossary of Parasitological Terms, see Annex section A7.25 A er the meeting, the experts developed informative summaries for the resulting 24 ranked parasites, for use by risk managers or any interested stakeholder. A glossary was also provided by the expert group to help the reader with the terminology.

A7.1 ANISAKIDAE AND ANISAKIASIS General information Anisakiasis refers to infection of people with nematode larvae belonging to the nematode Family Anisakidae, and it is a serious zoonotic disease. Although there are several zoonotic species in this family, the two species most o en associated with anisakiasis are Anisakis simplex the ‘herring worm’ and Pseudoterranova decipiens, the ‘cod worm’ (Chai, Murrell and Lymbery, 2005). e complex life history of A. simplex involves a marine intermediate host (euphasid crustacean), a paratenic host (marine sh or squid) and a de nitive host (marine mammal). Anisakiasis occurs when people ingest third-stage larvae that occur in the viscera or muscle of a wide range of marine sh and squids. Humans are accidental intermediate hosts in which the parasites rarely develop further; this invasion can cause gastrointestinal abscesses.

Geographical distribution Anisakiasis occurs throughout the world, but is reported most frequently from Asia (especially Japan) and Western Europe, where risky food behaviour customs (i.e., eating raw, lightly cooked, or marinated sh in dishes such as sushi, salted or smoked herring, gravlax, and ceviche) are common (Lymbery and Cheah, 2007). Recent molecular genetic studies have shown that these species, A. simplex and P. decipiens, actually comprise a number of sibling species, o en with distinct geographical and host ranges, or both (Mattiucci et al., 2005). Within the Anisakis simplex complex are: A. simplex (sensu stricto), found in the northern Atlantic; A. simplex C, found in the northern Paci c and southern waters below 30°N; and

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A. pegre , found in the Mediterranean Sea. ree species have also been described for the Pseudoterranova decipiens complex: P. decipiens A in the northeast Atlantic and Norwegian Sea, P. decipiens C in the northwest Atlantic and Barents Sea, and P. decipiens B throughout northern waters. Where the ranges of these species overlap, they appear to preferentially utilize di erent de nitive host species. Historically, most authors estimate there have been 15 000 to 20 000 total human cases. ere has been an increase in reported prevalence throughout the world in the last two decades, probably due to better diagnostic tools, increased demand for seafood, and a growing demand for raw or lightly cooked food, although none of these factors has been rigorously evaluated. e areas of highest prevalence are Japan (a er eating sushi and sashimi), and along the Paci c coast of South America (from eating ceviche, seviche or cebiche).

Disease When humans eat infected sh harbouring live third-stage larvae, the larvae migrate to the gastrointestinal mucosa, where they die, but induce the formation of abscesses. Presumptive diagnosis in humans may be made on the basis of the patient’s recent food habits (Gutierrez, 2011). De nitive diagnosis requires demonstration of worms by gastroscopy or surgery. No treatment is recommended for transient infection. In the gastrointestinal form (embedded larvae), surgery or gastroscopic procedure is also curative. ere is little information on chronic morbidity. However, the development of allergy to the parasite’s allergens (even when the sh is thoroughly cooked) is now recognized. Gastroallergic anisakiasis is an acute IgE-mediated generalized reaction, manifested by urticaria and anaphylaxis, with or without accompanying gastrointestinal symptoms (Audicana and Kennedy, 2008). Occupational allergy, including asthma, conjunctivitis and contact dermatitis, has also been observed in sh-processing workers. ere is little information available on illness fraction or case fatality rates, probably because most cases are acute and treated.

Trade relevance Anisakid infections are a trade issue because of regulations imposed by countries on imports. Many countries have regulations requiring inspection of sh for zoonotic parasites, and for inactivating any nematode larvae, etc., that may be present. Regulations and inactivation methods may di er in speci cs between countries. (See EU, no date; and Chapter 5 in FDA, no date).

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Impact on economically vulnerable populations Developing countries can be a ected by the necessity of taking steps to ensure sh exports are free of live anisakids. e inactivation methods described above can be expensive, and when not completely successful lead to rejection of exports by importing countries, especially fresh sh products.

References Audicana, M.T. & Kennedy, M. 2008. Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clinical Microbiology Reviews, 21(2): 360–379. Chai, J.Y., Murrell, K.D. & Lymbery, A.J. 2005. Fish-borne parasitic zoonoses: status and issues. International Journal for Parasitology, 35(11-12): 1233–1254. EU. No date. EU import conditions for seafood and other shery products. Web site. Available at http://ec.europa.eu/food/international/trade/im_cond_ sh_en.pdf Accessed 2013-06-23. FDA (Federal Drug Administration). No date. Chapter 5 – Parasites, in: Fish and Fishery Products Hazards and Controls Guidance. 4th Edition, November 2011. Available at http://www.fda.gov/downloads/Food/GuidanceRegulation/UCM252393.pdf Accessed 2013-08-24 Gutierrez, Y. 2011. Anisakidae. pp. 778–787 (Ch. 12), in: R.L. Guerrant, D.H. Walker and P.F. Weller (editors). Tropical Infectious Diseases: Principles, Pathogens and Practice. 3rd edition. Saunders, Philadelphia, USA. Lymbery, A.J. & Cheah, F.Y. 2007. Anisakid nematodes and anisakiasis. pp. 185–207, in: K.D. Murrell and B. Fried (editors). Food-borne parasitic zoonoses. Springer, New York, USA. Mattiucci, S., Nascetti, G., Dailey, M., Webb, S.C., Barros, N.B., Cianchi, R. & Bullini, L. 2005. Evidence for a new species of Anisakis Dujardin, 1845: morphological description and genetic relationships between congeners (Nematoda: Anisakidae). Systematic Parasitology, 61(3): 157–161.

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A7.2 ASCARIS SPP. General information Ascaris lumbricoides is the large intestinal roundworm (nematode) of humans, and the infection is termed ‘ascariasis’ or ‘ascariosis’, and rarely ‘ascarosis’. ‘Ascariasis’ is the most widely used, and will be used here. e adult worms are large (females up to 35 cm, males up to 31 cm in length), and individual worms can weigh as much as 7 or 8 g (Elkins and Haswellelkins, 1989). e adults occupy the small intestine and the female lays large numbers of eggs (estimated to be in the hundreds of thousands of eggs per day per female) (Brown and Cort, 1927; O’Lorcain and Holland, 2000). e eggs are voided in the faeces and are sticky, thick shelled and highly persistent in the environment such that they can survive for several years in soil. ey contaminate water supplies following rain or ooding, vegetables either directly from soil or by irrigation, and probably the hands and clothing of agricultural workers or other people in contact with contaminated soil. e practice of using human faeces as fertilizer in subsistence farming presents a signi cant risk of continued transmission. Ascaris suum is the large roundworm of pigs and is considered to be a separate species from A. lumbricoides. e two species are virtually indistinguishable morphologically, immunologically and biochemically, although there are some distinguishing immunological and biochemical features (e.g. Kennedy et al., 1987). DNA-based surveys have indicated that A. suum is mostly con ned to pigs, and A. lumbricoides to humans, but that there is evidence of cross-infections such that A. suum may present a signi cant risk to humans Peng and Criscione, 2012; Zhou et al., 2012; Nejsum et al., 2005). In regions endemic for both parasites it appears mostly, but not exclusively, to be the case that adult worms of A. lumbricoides have a host preference for humans, and adult worms of A. suum have a host preference for pigs (Peng and Criscione, 2012). In regions where A. lumbricoides does not occur in humans, there have been cases of infection with A. suum that have been attributed to contamination from pig farms (Nejsum et al., 2005; Anderson, 1995). In both species, infection occurs by ingestion of viable eggs, which hatch in the small intestine, releasing the infective-stage larvae of the parasite, which is in its third developmental stage (L3). e larvae then undergo a tissue migration involving the liver then the lungs. In the lungs the larvae break through to the air spaces, migrate up the trachea, are then swallowed and thereby re-introduced to the gastrointestinal tract, where they mature to adult worms in the small intestine. e global prevalence of human ascariasis in the 1990s was estimated to be approximately 1.5 billion with 100–200 million people a ected clinically, a large proportion of whom were children (reviewed in O’Lorcain and Holland (2000) and

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Peng and Criscione (2012). More recent estimates are slightly lower at 1.2 billion people infected, which is largely due to China’s large-scale treatment programmes (reviewed in O’Lorcain and Holland (2000) and Peng and Criscione (2012)), but some estimates remain as high as 2 billion people currently infected.

Geographical distribution e distribution of both species of Ascaris is essentially global, but with low prevalences in countries with well-developed sanitation systems, and very high prevalences in regions with poor sanitation. e greater association with tropical and subtropical countries may merely be because many of these have poorer overall sanitation systems and parasite control programmes, and the viability and development to infectivity of eggs is favoured under warm, moist conditions. Exposure of humans to eggs of A. suum will be less likely in regions where pigs are not farmed.

Disease Ascariasis in humans presents mainly in the gut (small intestine and ileum) and the lungs, though larval migration through the liver and peritoneum likely also cause damage (O’Lorcain and Holland, 2000). In the gut, the worms can occur in such numbers that blockage and rupture or perforation can occur in extreme cases. e parasites have also been known to cause death by migrating into and blocking the pancreatic or bile ducts. e worms in the gut can cause malabsorption and anorexia, which will contribute to malnutrition (O’Lorcain and Holland, 2000). e malabsorption may be due to a loss of brush border enzymes, erosion and attening of the villi, and in ammation of the lamina propria, and premature cessation of lactase production has also been intimated (O’Lorcain and Holland, 2000). Migration of larvae through the lungs can cause severe immune hypersensitivity responses (Loe er’s Syndrome) that may be life-threatening. is appears to be more common in arid areas when periodic rains mobilise dormant Ascaris eggs from soil and other sources such as latrines, resulting in a high level of contamination of water and food supplies. It is highly likely that severe pulmonary reactions can be caused by exposure to the eggs of either A. lumbricoides or A. suum (as is known in sheep and cattle from exposure to A. suum eggs, and in experimentally infected animals such as rats, mice and rabbits, the larvae of either species reach the lungs). Infection with adult Ascaris can be detected by observation of eggs in faeces, although this requires the presence of a reproductive female. A. suum infections of humans in developed countries is o en with single or low numbers of worms. Loe er’s Syndrome can be detected by X-ray appearance of shadows on the lungs (Loe er, 1956), and detection of larvae and eosinophils in sputum or throat swabs. A characteristic feature of infection with parasitic worms is high levels of IgE antibody and eosinophils in blood, and eosinophils and mast cells in infected tissues; there is evidence that allergic-type immune responses may be part

ANNEX 7 SPECIFIC INFORMATION FOR THE RANKED PARASITES

of the protective response to Ascaris (McSharry et al., 1999). Important allergens have been described from Ascaris. See O’Lorcain and Holland (2000) for further detail on ascariasis disease symptoms and other e ects.

Trade relevance Contamination of fresh produce with Ascaris eggs has not been an issue in trade up to now. e main risk here is through fresh vegetables that have been contaminated with eggs directly from the soil in which they were grown, or the water with which they were irrigated or treated and prepared post-harvest. Trade in pigs can clearly also be a source of infection to new areas. e robustness of Ascaris eggs means that they can survive for long periods during transport, and they can survive low temperatures, including freezing to some degree, desiccation and chemical attack, though not cooking. Once soil is contaminated with viable eggs, it can remain so for up to a decade.

Impact on economically vulnerable populations e potential impact of ascariasis is chronic and insidious for communities, and can be severe and even life-threatening for individuals. In addition to the overt disease symptoms due to A. lumbricoides infection detailed above, there is evidence that chronic infection can a ect the growth rate and nal height, of children, and their cognitive development (reviewed in O’Lorcain and Holland, 2000, and Bundy, Walson and Watkins, 2013), which is likely to be particularly so in double or multiple infections with other species of worm parasites. In regions where pigs are kept, the risks of intestinal infection with adult A. suum may be low, but migratory larvae will still cause damage to liver and lungs, and it is likely that the risk of Loe er’s Syndrome will be similar with either species of Ascaris. Lamentably little research has been carried out on the prevalence, morbidity and mortality due to Loe er’s Syndrome or less acute but chronic, repetitive damage to the lungs, in humans infected with either parasite. is paucity of information on the pulmonary stage of infection is particularly unfortunate given the possibility that lung damage could exacerbate lung infections and consequent mortality in children (O’Lorcain and Holland, 2000).

Other relevant information Drugs for the treatment for the intestinal stage of ascariasis are cheap, readily available and relatively free of side-e ects. Treatments for the tissue migratory phases would be rare, partly because of the di culty of diagnosis, and possibly also the risk of causing deleterious reactions to dead larvae in liver, lungs or elsewhere (O’Lorcain and Holland, 2000). ere are no vaccines available against ascariasis. ere continues to be a debate about whether infection with Ascaris or other helminth parasites increases or decreases the risk of allergic reactions to environmental allergens (Pinelli et al., 2009). 68 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

References General sources Holland, C.V. (Editor). 2013. Ascaris: e Neglected Parasite. CABI Publishing, Wallingford, Oxfordshire, UK, and Cambridge, MA, USA.

Speci c sources cited Anderson, T.J.C. 1995. Ascaris infections in humans from North America – molecular evidence for cross-infection. Parasitology, 110: 215–219. Brown, H.W. & Cort, W.W. 1927. Parasitology, 14: 88–90. e egg production of Ascaris lumbricoides. Journal of

Bundy, D.A.P., Walson, J.L. & Watkins, K.L. 2013. Worms, wisdom, and wealth: why deworming can make economic sense. Trends in Parasitology, 29: 142–148. Elkins, D.B. & Haswellelkins, M. 1989. e weight-length pro les of Ascaris lumbricoides within a human community before mass treatment and following re-infection. Parasitology, 99: 293–299. Kennedy, M.W., Qureshi, F., Haswellelkins, M. & Elkins, D.B. 1987. Homology and heterology between the secreted antigens of the parasitic larval stages of Ascaris lumbricoides and Ascaris suum. Clinical and Experimental Immunology, 67: 20–30. Loe er, W. 1956. Transient lung in ltrations with blood eosinophilia. International Archives of Allergy and Applied Immunology, 8: 54–59. McSharry, C., Xia, Y., Holland, C.V. & Kennedy, M.W. 1999. Natural immunity to Ascaris lumbricoides associated with immunoglobulin E antibody to ABA-1 allergen and in ammation indicators in children. Infection and Immunity, 67: 484–489. Nejsum, P., Parker, E.D. Jr, Frydenberg, J., Roepstor , A., Boes, J., Haque, R., Astrup, I., Prag, J. & Skov Sørensen, U.B. 2005. Ascariasis is a zoonosis in Denmark. Journal of Clinical Microbiology, 43(3): 1142–1148. O’Lorcain, P. & Holland, C.V. 2000. Parasitology, 121: S51–S71. e public health importance of Acaris lumbricoides.

Peng, W. & Criscione, C.D. 2012. Ascariasis in people and pigs: new inferences from DNA analysis of worm populations. Infection Genetics and Evolution, 12: 227–235. Pinelli, E., Willers, S.M., Hoek, D., Smit, H.A., Kortbeek, L.M., Hoekstra, M., de Jongste, J., van Knapen, F., Postma, D., Kerkhof, M., Aalberse, R., van der Giessen, J.W. & Brunekreef, B. 2009 Prevalence of antibodies against Ascaris suum and its association with allergic manifestations in 4-year-old children in e Netherlands: the PIAMA birth cohort study. European Journal of Clinical Microbiology & Infectious Diseases, 28(11): 1327–1334. Zhou, C., Li, M., Yuan, K., Deng, S. & Peng, W. 2012. Pig Ascaris: an important source of human ascariasis in China. Infection Genetics and Evolution, 12: 1172–1177. ANNEX 7 SPECIFIC INFORMATION FOR THE RANKED PARASITES

A7.3 BALANTIDIUM COLI General information Balantidium coli is a protozoan parasitic species that causes the disease balantidiasis (CDC, no date; Anon., 2003). It is the only member of the ciliate phylum known to be pathogenic to humans (CDC, no date; Anon., 2003a). Infection occurs when the cysts are ingested, usually through contaminated food or water. is parasite lives in the caecum and colon of humans. B. coli has two developmental stages, a trophozoite stage and a cyst stage. Trophozoites multiply and encyst due to the dehydration of faeces. It can thrive in the gastrointestinal tract as long as there is a balance between the protozoan and the host without causing dysenteric symptoms. Infection most likely occurs in people with malnutrition due to the low stomach acidity or people with immune compromised systems (Anon., 2003b; Schuster and Ramirez-Avila, 2008).

Geographical distribution e disease is considered to be rare and occurs in less than 1% of the human population. Most infections occur in developing countries where faeces are more likely to get in contact with food and drinking water. In addition to humans, pigs and other animals carry the disease. People who raise pigs have a greater risk of getting infected with balantidiasis. Co-infections with other parasites are likely to aggravate the damage wrought by each individual parasite, and they probably share common sources of infection (i.e. contaminated water) (Roberts and Janovy, 2009). Balantidiasis in humans is common in the Philippines, but it can be found anywhere in the world, especially among those that are in close contact with swine. It has been noted in Latin America, Bolivia, Southeast Asia and New Guinea.

Disease Common symptoms of balantidiasis include chronic diarrhoea, occasional dysentery (diarrhoea with passage of blood or mucus), nausea, foul breath, colitis (in ammation of the colon), abdominal pain, weight loss, deep intestinal ulcerations, and possibly perforation of the intestine. Fulminating acute balantidiasis is when the disease comes very suddenly and with great intensity. Haemorrhaging can occur, which can lead to shock and death. Untreated fulminating acute balantidiasis is reported to have a fatality rate of 30%. In acute disease, explosive diarrhoea may occur as o en as every twenty minutes. Perforation of the colon may also occur in acute infections which can lead to life-threatening situations. If balantidiasis is not treated the persistent diarrhoea leads to high uid loss and dehydration. If abdominal bleeding occurs, it can lead to death (Schuster and Ramirez-Avila, 2008).

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Trade relevance ere have not yet been signi cant trade issues with respect to ndings of B. coli in foods, but with the increasing number of surveillance studies reporting positive results worldwide, and the growing number of produce-associated illness outbreaks, more trade issues resulting in import restrictions and recalls may occur in the future. B. coli causes reduced production performance in the animals a ected, which has an impact on the economy, both locally for farmers and nationally for the country (Roberts and Janovy, 2009).

Impact on economically vulnerable populations e disease is a problem primarily in developing countries, where water sources may be contaminated with swine or human faeces. Balantidiasis infections can be prevented by following appropriate hygiene practices (such as not using human faeces as fertilizer in agriculture; washing hands a er going to the toilet and before meals; washing vegetables; and cooking meat properly). Infective B. coli cysts are killed by heat (Schuster and Ramirez-Avila, 2008).

References Anon[ymous]. 2003a. e Parasite: Balantidium coli. e Disease: Balantidiasis. Introduction. Web site prepared by A. Ramachandran. Last updated 2003-05-23; accessed 2013-06-18. Online at http://www.stanford.edu/group/parasites/ParaSites2003/Balantidium/Balantidium_coli_ParaSite.htm. Anon. 2003b. e Parasite: Balantidium coli. e Disease: Balantidiasis. Morphology. Web site prepared by A. Ramachandran. Last updated 2003-05-23; accessed 201306-18. Online at http://www.stanford.edu/group/parasites/ParaSites2003/Balantidium/Morphology.htm CDC (Centres for Disease Control and Prevention). No date. Parasites and Health: Balantidiasis [Balantidium coli]. Online. See: http://www.dpd.cdc.gov/dpdx/HTML/ Balantidiasis.htm Accessed 2013-06-18. Schuster, F.L. & Ramirez-Avila, L. 2008. Current world status of Balantidium coli. Clinical Microbiology Review, 21(4): 626–638. Roberts, L.S. & Janovy, J. Jr. 2009. Foundations of Parasitology. 8th Edition. McGrawHill, New York, USA.

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A7.4 CRYPTOSPORIDIUM SPP. General information Cryptosporidium spp. are protozoan parasites reported worldwide in a large number of di erent hosts, including humans. e infectious stages of Cryptosporidium spp., known as oocysts, are shed with the faeces of the host and can survive for long periods under cool and moist conditions. Routes of transmission include waterborne, person-to-person, zoonotic and foodborne. e waterborne route is numerically the most important means of transmission of cryptosporidiosis. Numerous waterborne outbreaks of cryptosporidiosis have occurred worldwide as a result of oocyst contamination of drinking water sources and recreational water. e largest waterborne illness outbreak of any kind in the United States of America occurred in the spring of 1993, when an estimated 403 000 people became ill with cryptosporidiosis in Milwaukee, Wisconsin. Foodborne transmission of cryptosporidiosis is thought to be much less common than waterborne or person-to-person transmission; about 8% of domestically acquired cases in the United States of America are food-borne (Scallan et al., 2011). It is, however, emerging as an important public health issue. Food-borne outbreaks of cryptosporidiosis associated with the consumption of fresh produce have been reported mainly in the United States of America and in northern Europe (Dixon et al., 2011; Robertson and Chalmers, 2013). e foods implicated in these outbreaks have included green onions, sandwich-bar ingredients, parsley, carrots, red peppers, and lettuce. In some cases these outbreaks were attributed to infected food-handlers. A large outbreak a ecting approximately 300 people occurred in the UK in 2012 and was associated with the consumption of pre-cut bagged salad products (HPA, 2013). ere have also been four cryptosporidiosis outbreaks associated with drinking unpasteurized apple cider, all in the United States of America. Unpasteurized milk has been associated with outbreaks of cryptosporidiosis in Australia and the UK. Chicken salad was implicated in an outbreak in the United States of America and may have been contaminated by a food worker who also operated a daycare facility. Numerous surveys performed worldwide have reported the presence of Cryptosporidium oocysts on a wide variety of fresh produce items (Dixon et al., 2013). Cryptosporidium oocysts have also been reported worldwide in the gills and tissues of oysters and other molluscan shell sh, including clams, cockles and mussels (Fayer, Dubey and Lindsay, 2004).

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Control measures to reduce the likelihood of contamination of produce at the preharvest stage with Cryptosporidium include the use of good quality water for irrigation, mixing of pesticides, or washing and processing; restricting access of livestock and other animals to crop lands and surface waters; monitoring the health of farm workers and encouraging good hygiene; and using only composted manure as fertilizer. Post-harvest control measures include the use of good quality water for washing and processing produce; monitoring and enforcing good personal hygiene in food handlers; prevention of cross-contamination; and the incorporation of HACCP plans. At the consumer level, good hygiene and avoidance of crosscontamination are again important control measures. orough washing of fresh produce is recommended, but probably will not be fully e ective in removing all contaminating oocysts. Although oocysts are somewhat resistant to freezing, they can be inactivated by storing produce at -20°C for >24 hours, or at -15°C for at least a week. Alternatively, oocysts will be readily destroyed in foods that are subsequently cooked.

Geographical distribution In recent years, human infection with Cryptosporidium spp. has emerged as a global public health problem. Prevalence, however, is very di cult to determine as data is not available from many countries. In one estimate, the prevalence of Cryptosporidium in patients with gastroenteritis was 1–4% in Europe and North America, and 3–20% in Africa, Asia, Australia, and South and Central America (Current and Garcia, 1991). Laberge and Gri ths (1996) estimated that the prevalence rates based on oocyst excretion were 1–3% in industrialized countries, and up to 10% in developing countries. Cryptosporidiosis has been reported in 106 countries worldwide (Fayer, 2008). Approximately twelve species of Cryptosporidium, and several genotypes, have been reported in humans. However, 90% of reported human infections involve C. hominis, which is found primarily in humans, and C. parvum, which is an important zoonotic species. C. hominis is thought to account for more human cases than C. parvum in North America, Australia, Asia, sub-Saharan Africa and some parts of Europe. Generally speaking, C. parvum is more prevalent in rural or agricultural regions, probably as a result of zoonotic transmission. In recent years, C. meleagridis has been reported more commonly in humans. For example, Cama et al. (2008) reported a relatively high prevalence of infection with C. meleagridis in children in Peru. Similarly, C. cuniculus was found to be the third most commonly identi ed species, a er C. parvum and C. hominis, in sporadic cases of cryptosporidiosis in the UK (Chalmers et al., 2011). Several other Cryptosporidium species and genotypes are only occasionally found in humans (Xiao, 2010).

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Disease Cryptosporidiosis is an enteric disease which is self-limiting in immunocompetent individuals. e disease is characterized by watery diarrhoea and a variety of other symptoms, including, abdominal pain, weight loss, nausea, vomiting, fever and malaise (Chalmers and Davies, 2010). Symptoms in some immunocompromised patients become chronic, debilitating and potentially life-threatening. Cryptosporidiosis accounts for up to 6% of all reported diarrhoeal illnesses in immunocompetent persons (Chen et al., 2002). Twenty-four percent of AIDS patients with diarrhoea are infected with Cryptosporidium spp. (Guerrant, 1997). In the United States of America, Scallan et al. (2011) reported a hospitalization rate of 25%, and a death rate of 0.3%, in laboratory-con rmed cases of cryptosporidiosis. In addition to the patients’ immune status, there is some evidence that clinical manifestations of cryptosporidiosis may also be partially dependent upon the species of Cryptosporidium involved in the infection. With the exception of Nitazoxanide, which is approved in the United States of America for treating diarrhoea caused by Cryptosporidium in immunocompetent patients, drug development has been largely unsuccessful against cryptosporidiosis.

Trade relevance ere have not yet been signi cant trade issues with respect to the nding of Cryptosporidium oocysts in foods, but with the increasing number of surveillance studies reporting positive results in a wide variety of foods worldwide, and the growing number of produce-associated illness outbreaks, more trade issues resulting in import restrictions and recalls may occur in the future. As has already been seen with respect to Cyclospora cayetanensis in fresh berries, these actions could have signi cant impacts on the agricultural industry and the economy of developing countries that produce and export fresh produce. An ISO international standard for the detection and enumeration of Cryptosporidium and Giardia in fresh leafy green vegetables and berry fruits is currently being dra ed and may have implications for trade in future as more standardized food testing is done.

Impact on economically vulnerable populations Along with giardiasis, cryptosporidiosis was included in the WHO Neglected Diseases Initiative in 2004. Diseases included in this initiative “occur mainly in developing countries where climate, poverty and lack of access to services in uence outcomes”, and where they “impair the ability of those infected to achieve their full potential, both developmentally and socio-economically” (Savioli, Smith and ompson, 2006). As such, cryptosporidiosis in particular may have considerable negative impacts on economically vulnerable populations.

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References Cama, V.A., Bern, C., Roberts, J., Cabrera, L., Sterling, C.R., Ortega, Y., Gilman, R.H. & Xiao, L. 2008. Cryptosporidium species and subtypes and clinical manifestations in children, Peru. Emerging Infectious Diseases, 14: 1567–1574. Chalmers, R. M. & Davies, A.P. 2010. Minireview: clinical cryptosporidiosis. Experimental Parasitology, 124: 138–146. Chalmers, R.M., Elwin, K., Had eld, S.J. & Robinson, G. 2011. Sporadic human cryptosporidiosis caused by Cryptosporidium cuniculus, United Kingdom, 2007–2008. Emerging Infectious Diseases, 17: 536–538. Chen, X.M., Keithly, J.S., Paya, C.V. & LaRusso, N.F. 2002. Cryptosporidiosis. New England Journal of Medicine, 346: 1723–1731. Current, W.L. & Garcia, L.S. 1991. Cryptosporidiosis. Clinical Microbiology Reviews, 4: 325–358. Dixon, B.R., Fayer, R., Santin, M., Hill, D.E. & Dubey, J.P. 2011. Protozoan parasites: Cryptosporidium, Giardia, Cyclospora and Toxoplasma. pp. 349–370, in: J. Hoorfar (editor). Rapid detection, characterization and enumeration of food-borne pathogens. ASM Press, Washington D.C., USA. Dixon, B., Parrington, L., Cook, A., Pollari, F. & Farber, J. 2013. Detection of Cyclospora, Cryptosporidium and Giardia in ready-to-eat packaged leafy greens in Ontario. Canada. Journal of Food Protection, 76: 307–313. Fayer, R. 2008. Biology. pp. 1–42, in: R. Fayer and L. Xiao (editors). Cryptosporidium and Cryptosporidiosis. 2nd edition. CRC Press and IWA Publishing, Boca Raton, FL, USA. Fayer, R., Dubey, J.P. & Lindsay, D.S. 2004. Zoonotic protozoa: from land to sea. Trends in Parasitology, 20: 531–536. Guerrant, R.L. 1997. Cryptosporidiosis: an emerging, highly infectious threat. Emerging Infectious Diseases, 3: 51–57. HPA (Health Protection Agency). 2012. Investigation into an outbreak of Cryptosporidium infection in spring 2012. Online HPA Press Release 2013-03-19. See: http:// www.hpa.org.uk/NewsCentre/ NationalPressReleases/2013PressReleases/130319I nvestigationintoanoutbreakofcryptosporidium/ Accessed 2013-06-18. Laberge, I. & Gri ths, M.W. 1996. Prevalence, detection and control of Cryptosporidium in food. International Journal of Food Microbiology, 32: 1–26. Robertson, L.J. & Chalmers, R.M. 2013. Food-borne cryptosporidiosis: is there really more in Nordic countries? Trends in Parasitology, 29: 3–9.

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Savioli, L., Smith, H. & ompson, A. 2006. Giardia and Cryptosporidium join the “Neglected Diseases Initiative”. Trends in Parasitology, 22: 203–208. Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., Jones, J.L. & Gri n, P.M. 2011. Food-borne illness acquired in the United States – major pathogens. Emerging Infectious Diseases, 17(1): 7–15. Xiao, L. 2010. Molecular epidemiology of cryptosporidiosis: an update. Experimental Parasitology, 124: 80–89.

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A7.5 CYCLOSPORA CAYETANENSIS General information Cyclospora cayetanensis is a coccidian parasite that can be acquired by ingestion of contaminated raw produce (vegetables, herbs and fruits) and possibly drinking water. Sporulated oocysts excyst in the gastrointestinal tract and invade the epithelial cells of the small intestine, where asexual and sexual multiplication occurs. Unsporulated oocysts are formed and excreted in the faeces of the infected individual. It takes 7–15 days under ideal environmental conditions for these oocysts to sporulate and become infectious. Oocysts measure 8–10 µm in diameter and auto uoresce when exposed to UV light. Sporulated oocysts consist of two sporocysts, each containing two sporozoites. C. cayetanensis seems to be speci cally anthroponotic. A few reports described Cyclospora oocysts in the faeces of dogs, ducks and chickens, but unsuccessful experimental infections and lack of histopathological evidence of infection do not support the availability of an intermediate or de nitive host other than human (Ortega and Sanchez, 2010) and these undoubtedly represented spurious passage of oocysts. In the past decade, other Cyclospora species have been described in non-human primates, but molecular information has con rmed that these species are not C. cayetanensis (Eberhard et al., 1999). In the United States of America, it is estimated that annually the mean number of episodes of gastroenteritis caused by Cyclospora is 11 407 (CI: 137–37 673) with a 6.5% hospitalization rate (Scallan et al., 2011). To date, no deaths have been reported due to Cyclospora infections and there is no evidence that Cyclospora is endemic in the United States of America. Waterborne transmission can occur (Rabold et al., 1994). Oocysts have been identi ed in water used for human consumption in various studies; however, foodborne transmission has been reported more frequently and has been linked to lettuce, basil, snow peas and berries (blackberries and raspberries) (Shields and Olson, 2003) that were consumed raw, and frequently associated with social events. In 1996, 1465 cases of cyclosporiasis, associated with consumption of Guatemalan raspberries, were reported in the United States of America and Canada. In 1997, 1012 more cases were reported associated with the consumption of Guatemalan raspberries, and 342 cases implicated contaminated basil. In 1998, raspberry importations were not permitted into the United States of America whereas importation into Canada continued. at year, 315 cases of cyclosporiasis were reported in Canada, again implicating raspberries imported from Guatemala (Herwaldt, 2000). Since then, Cyclospora cases have been reported in the United States of America every year, and in most instances no speci c food commodity has been associated with those outbreaks. Outbreaks of Cyclospora have also been reported in

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Europe (Doller et al., 2002). In most instances, reports from Europe describe cases associated with travel to endemic areas (Cann et al., 2000; Clarke and McIntyre, 1996; Green et al., 2000). In December 2000, 34 persons acquired cyclosporiasis in Germany. e food items implicated as a result of the epidemiological investigation (butterhead lettuce (from Southern France), mixed lettuce (from Bari, Italy), and chives (from Germany)) were not available for microbiological examination (Doller et al., 2002).

Geographical distribution Cyclospora has been reported to be endemic in China, Cuba, Guatemala, Haiti, India, Mexico, Nepal, Peru and Turkey. Other reports from travellers suggest that Cyclospora could also be endemic in other tropical regions, including Bali, Dominican Republic, Honduras, Indonesia, Papua New Guinea and ailand (Ortega and Sanchez, 2010). e prevalence of Cyclospora in these regions has changed as the socio-economic conditions of the populations have changed. ere are reports of infection in parts of Africa, but the absence of infection has been noted in many studies that looked speci cally for it, and further study and conrmation of the distribution of the organisms in this part of the world is required.

Disease Cyclosporiasis is characterized by watery diarrhoea, nausea, abdominal pain and anorexia. Low-grade fever, atulence, fatigue and weight loss have also been reported. Biliary disease, Guillain-Barrè Syndrome and Reiter’s Syndrome have been reported to follow Cyclospora infections (Ortega and Sanchez, 2010). e severity of illness is higher in children, the elderly, and immunocompromised individuals. Symptomatic cyclosporiasis is common in naïve (non-endemic) populations. Illness usually lasts 7–15 days, but in immunocompromised and a few immunocompetent individuals it can last up to 3 months (Bern et al., 2002). Recurrence has been reported in HIV patients. e drug of choice to control infection is trimethoprim sulfamethoxazole, but in patients who are allergic to sulfa, ciprooxacin has been used as an alternative treatment. If not treated, the host’s immune response should eventually control the infection (Pape et al., 1994). In endemic areas, children under 10 years frequently acquire the infection, and as they grow and have repeated exposures, infections can be less symptomatic and of shorter duration (Bern et al., 2000, 2002; Hoge et al., 1995; Ortega et al., 1993). e environmental conditions that favour Cyclospora endemicity are not fully elucidated, nor are the conditions that allow for a marked seasonality characteristic in locations where Cyclospora is endemic (Lopez et al., 2003; Madico et al., 1997; Schlim et al., 1999).

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Trade relevance and impact on economically vulnerable populations Cyclospora has a ected international trade and susceptible populations. is was very evident during the 1995–1997 outbreaks in the United States of America. Importation of berries (Herwaldt, 2000), particularly raspberries, was a ected, causing signi cant nancial losses to the producers, exporters and importers. In 1996, United States of America strawberry growers were a ected as it was assumed that cases of cyclosporiasis were linked with California strawberries. e California Strawberry Commission estimated that this false assumption led to US$ 16 million in lost revenue to the growers in California during the month of June in that year. Later it was determined that these outbreaks were associated with the consumption of imported Guatemalan raspberries (Herwaldt et al., 1997). In 1996, before the Cyclospora outbreaks occurred, the number of raspberry growers in Guatemala was estimated to be 85. By 2002, only 3 remained. For many growers the decision to leave the industry was based on losses due to the lack of foreign demand of their berries and export markets closures (Calvin, Flores and Foster, 2003). e losses resulting from these outbreaks were signi cant not only nancially but also for the reputation of the Guatemalan berry industry and the communities involved. e global burden and prevalence of this parasite worldwide need to be considered. Its e ect in global trade has been notorious in commodities imported from endemic areas. However, e ects on the economy and health of the population in endemic countries, where exports are not an element of consideration in terms of outbreaks in developed countries, need to be further studied.

References Bern, C., Hernandez, B., Lopez, M.B., Arrowood, M.J., De Merida, A.M. & Klein, R.E. 2000. e contrasting epidemiology of Cyclospora and Cryptosporidium among outpatients in Guatemala. American Journal of Tropical Medicine and Hygiene, 63: 231–235. Bern, C., Ortega, Y., Checkley, W., Roberts, J.M., Lescano, A.G., Cabrera, L., Verastegui, M., Black, R.E., Sterling, C. & Gilman, R.H. 2002. Epidemiologic di erences between cyclosporiasis and cryptosporidiosis in Peruvian children. Emerging Infectious Diseases, 8: 581–585. Calvin, L., Flores, L. & Foster, W. 2003. Case Study: Guatemalan raspberries and Cyclospora. Food Safety in Food Security and Food Trade series, Focus 10, Brief 7. Part of the 2020 Vision For Food, Agriculture, and the Environment programme. IFPRI, Washington DC, USA. See http://www.ifpri.org/sites/default/ les/publications/focus10_07.pdf Accessed 2013-06-18.

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Cann, K.J., Chalmers, R.M., Nichols, G. & O’Brien, S.J. 2000. Cyclospora infections in England and Wales: 1993 to 1998. Communicable Diseases and Public Health, 3: 46–49. Clarke, S.C. & McIntyre, M. 1996. e incidence of Cyclospora cayetanensis in stool samples submitted to a district general hospital. Epidemiology & Infection, 117: 189– 193. Doller, P.C., Dietrich, K., Filipp, N., Brockmann, S., Dreweck, C., Vonthein, R., Wagner-Wiening, C. & Wiedenmann, A. 2002. Cyclosporiasis outbreak in Germany associated with the consumption of salad. Emerging Infectious Diseases, 8: 992–994. Eberhard, M.L., da Silva, A.J., Lilley, B.G. & Pieniazek, N.J. 1999. Morphologic and molecular characterization of new Cyclospora species from Ethiopian monkeys: C. cercopitheci sp.n., C. colobi sp.n., and C. papionis sp.n. Emerging Infectious Diseases, 5: 651–658. Green, S. T., McKendrick, M.W., Mohsen, A.H., Schmid, M.L. & Prakasam, S.F. 2000. Two simultaneous cases of Cyclospora cayatensis enteritis returning from the Dominican Republic. Journal of Travel Medicine, 7(1): 41–42. Herwaldt, B.L. 2000. Cyclospora cayetanensis: a review, focusing on the outbreaks of cyclosporiasis in the 1990s. Clinical Infectious Diseases, 31(4): 1040–1057. Herwaldt, B.L., Ackers, M.L. and 52 others [ e Cyclospora Working Group]. 1997. An outbreak in 1996 of cyclosporiasis associated with imported raspberries. New England Journal of Medicine, 336(22): 1548–1556. Hoge, C.W., Echeverria, P., Rajah, R., Jacobs, J., Malthouse, S., Chapman, E., Jimenez, L.M. & Shlim, D.R. 1995. Prevalence of Cyclospora species and other enteric pathogens among children less than 5 years of age in Nepal. Journal of Clinical Microbiology, 33: 3058–3060. Lopez, A.S., Bendik, J.M., Alliance, J.Y., Roberts, J.M., da Silva, A.J., Moura, I.N., Arrowood, M.J. Eberhard, M.L. & Herwaldt, B.L. 2003. Epidemiology of Cyclospora cayetanensis and other intestinal parasites in a community in Haiti. Journal of Clinical Microbiology, 41: 2047–2054. Madico, G., McDonald, J., Gilman, R.H., Cabrera, L. & Sterling, C.R. 1997. Epidemiology and treatment of Cyclospora cayetanensis infection in Peruvian children. Clinical Infectious Diseases, 24(5): 977–981. Ortega, Y.R. & Sanchez, R. 2010. Update on Cyclospora cayetanensis, a food-borne and waterborne parasite. Clinical Microbiology Reviews, 23: 218–234. Ortega, Y.R., Sterling, C.R., Gilman, R.H., Cama, V.A. & Diaz, F. 1993. Cyclospora species – a new protozoan pathogen of humans. New England Journal of Medicine, 328(18): 1308–1312.

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Pape, J.W., Verdier, R.I., Boncy, M., Boncy, J. & Johnson, W.D. Jr. 1994. Cyclospora infection in adults infected with HIV. Clinical manifestations, treatment, and prophylaxis. Annals of Internal Medicine, 121: 654–657. Rabold, J.G., Hoge, C.W., Shlim, D.R., Ke ord, C., Rajah, R. & Echeverria, P. 1994. Cyclospora outbreak associated with chlorinated drinking water. Lancet, 344: 1360– 1361. Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., Jones, J.L. & Gri n, P.M. 2011. Food-borne illness acquired in the United States – major pathogens. Emerging Infectious Diseases, 17:7-15. Shields, J.M. & Olson, B.H. 2003. Cyclospora cayetanensis: a review of an emerging parasitic coccidian. International Journal of Parasitology, 33: 371–391. Shlim, D.R., Hoge, C.W., Rajah, R., Scott, R.M., Pandy, P. & Echeverria, P. 1999. Persistent high risk of diarrhea among foreigners in Nepal during the rst 2 years of residence. Clinical Infectious Diseases, 29: 613–616.

CHAPTER 1 INTRODUCTION

A7.6 DIPHYLLOBOTHRIUM SPP. General information Human diphyllobothriasis is a sh-borne zoonosis distributed worldwide and it is transmitted by cestodes belonging to the genus Diphyllobothrium. e life cycle of these tapeworms involves two intermediate hosts (zooplankton and some marine and freshwater sh species, especially those anadromous species that migrate from salt to fresh water to spawn), and piscivorous mammals and birds as de nitive hosts. Fourteen of the 50 known species of Diphyllobothrium so far described are known to infect humans (Scholz et al., 2009). e occurrence of the disease is closely linked to the consumption of raw or undercooked freshwater or marine shes. Diphyllobothriasis is considered a mild illness and is not reportable, therefore the estimates of global illnesses attributed to this sh-borne zoonosis are based on limited human surveys and clinical case reports. Chai, Murrell and Lymbery (2005) estimated global infection at 20 million. Dorny and co-workers (2009) estimated that in about 20% of the infections, clinical manifestations occur.

Geographical distribution Americas Until 1982, diphyllobothriasis was a reportable disease in the United States of America, with 125–200 cases reported during the period 1977–1981 (Ruttenber et al., 1984). In North America, most cases occur in the Great Lakes region and Alaska, although cases have been reported elsewhere (Cushing and Bacal, 1934; Margolis, Rausch and Robertson, 1973; Turgeon, 1974). e following species of Diphyllobothrium were documented as infecting humans in North America: D latum, D dendriticum, D. dalliae, D. lanceolatum, D. ursi, D. alascense and, just recently, D. nihonkaiense (reviewed by Scholz et al., 2009). Human infections are commonly reported within the Southern Cone of South America, most commonly with D. latum and D. paci cum (Mercado et al., 2010), which includes Chile (Mercado et al., 2010; Torres et al., 1993), Argentina (Semenas, Kreiter and Urbanski, 2001) and Peru (Lumbreras et al., 1982) on the Paci c coast. In Chile, 0.4–1.4% of the population shed Diphyllobothrium eggs in high-risk zones (Torres et al., 1993; Navarrete and Torres, 1994). Asia In Japan, it is estimated that, on average, about 100 cases per year of diphyllobothriasis occur (Oshima and Kliks, 1987), and in the Republic of Korea, at least 47 cases have been reported since 1971 (Lee et al., 2007; Jeon et al., 2009), most commonly with D. nihonkaiense. In China, 12 cases (Guo et al., 2012) of infection

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with D. latum were reported in 2009–2011; however, these gures are likely to be a gross underestimate of true incidence. Sporadic reports of clinical illness have also been reported in Malaysia (Rohela et al., 2002, 2006), India (Devi et al., 2007; Duggal et al., 2011; Ramana et al., 2011) and Taiwan (Chou et al., 2006; Lou et al., 2007). In easternmost Russia, where D. klebanovskii is considered the important zoonotic species, human prevalence usually ranges from 1.0 to 3.3%. Since the completion of the Krasnoyaek Reservoir on the Enisel River the prevalence of D. klebanovskii has risen as high as 7.7% in people living along the reservoir shore (Scholz et al., 2009; Chai, Murrell and Lymbery, 2005). Europe D. latum has been considered to be the principal species infecting humans in Europe, with D. dendriticum present in northern Europe. e incidence appears to be on the decline overall. In Scandinavian countries it persists in several regions. Currently Switzerland, Sweden, Finland and Estonia report more than 10 cases per year (440 in Estonia in 1997), while Lithuania, Poland, Hungary, Italy and France average 2–10 cases annually. Only sporadic cases occur in Norway, Austria and Spain. Over 30 cases have been identi ed on the Swiss shores of Lake Maggiore since 1990, and 70 cases on the Swiss and French shores of Lake Leman between 1993 and 2002 (Dupouy-Camet and Peduzzi, 2004).

Disease Severity of acute morbidity Acutely, patients may experience vomiting, abdominal discomfort, cramps, diarrhoea and shed ribbon-like proglottids in their faeces (Lumbreras et al., 1982; Ramana et al., 2011; Wicht et al., 2008). Severity of chronic morbidity is was reviewed by Scholtz et al. (2009). In addition to chronic relapsing diarrhoea and abdominal discomfort (Wicht et al., 2008; Choi, Lee and Yang, 2012), prolonged or heavy infection may cause megaloblastic anaemia due to a parasite-mediated dissociation of the vitamin B12-intrinsic factor complex within the gut lumen, making B12 unavailable to the host. Approximately 80% of the B12 intake is absorbed by the worm, with a di erential absorption rate of 100:1 in relation to absorption by the host (Scholz et al., 2009). Chronic illness fraction About 40% of infected individuals may show low B12 levels, but only 2% or less develop clinical anaemia, which is hyperchromic and macrocytic and may be associated with low platelets or low white blood cell counts (Scholz et al., 2009). is de ciency may produce damage to the nervous system, including peripheral neuropathy or central nervous system degenerative lesions (Scholz et al., 2009). ANNEX 7 SPECIFIC INFORMATION FOR THE RANKED PARASITES

Case fatality rates No reports. Increase in human illness potential Increased human illness is unlikely with regards to severity, but is potentially an emerging zoonosis due to increased globalization associated with travel and trade, as well as increases in global popularity of eating dishes such as sushi and sashimi. Risks are mostly associated with wild-caught sh given the primarily sylvatic nature of the parasite’s life cycle.

Trade relevance As the demands for ‘premium’ quality sh and shery products increase, harvesting and export of wild-caught sh from diphyllobothriid-endemic areas that are transported chilled (not frozen) pose the greatest risk to trade (Chetrick, 2007). Inactivation of larvae (plerocercoids) requires cooking sh at 55°C for at least 5 minutes, or freezing it at -18°C for at least 24 h before consumption. An increasing number of human cases of diphyllobothriasis due to ‘exotically’ located Diphyllobothrium species are being reported (de Marval et al., 2013). To date, D. nihonkaiense infection has been reported in three Swiss (Wicht, de Marval and Peduzzi, 2007; Shimizu et al., 2008) and two French locals (Paugam et al., 2009; Yera et al., 2006) and a case of D. dendriticum (de Marval et al., 2013) in a Swiss local that had most likely consumed salmon imported from Finland (Wicht et al., 2008).

Impact on economically vulnerable populations True incidence and contribution to morbidity remain unascertained. e zoonosis is likely to have impacts, especially within developing communities, due to the neglected nature of parasitism.

Other relevant information In those areas where mass drug administration programmes are carried out and known to be endemic for diphyllobothriasis, it may be important to consider the inclusion of praziquantel and educational measures aimed at discouraging the practice of eating insu ciently cooked sh.

References Chai, J.Y., Murrell, K.D. & Lymbery, A.J. 2005. Fish-borne parasitic zoonoses: status and issues. International Journal for Parasitology, 35(11-12): 1233–1254. Chetrick, J. 2007. Sales of premium products to EU drive record U.S. seafood exports. FAS Worldwide, March 2007: 1–3. Online. Available at https://www.fas.usda.gov/ info/fasworldwide/2007/03-2007/EUSeafood.pdf Accessed 2013-06-20. 84

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Choi, H.J., Lee, J. &Yang, H.J. 2012. Four human cases of Diphyllobothrium latum infection. Korean Journal of Parasitology, 50(2): 143–146. Chou, H.F., Yen, C.M., Liang, W.C. & Jong, Y.J. 2006. Diphyllobothriasis latum: the rst child case report in Taiwan. Kaohsiung Journal of Medical Science, 22(7): 346–351. Cushing, H.B. & Bacal, H.L. 1934. Diphyllobothrium latum (Fish Tapeworm) infestation in eastern Canada with particular reference to its increasing prevalence. Canadian Medical Association Journal, 30(4): 377–384. de Marval, F., Gottstein, B., Weber, M. & Wicht, B. 2010 Imported diphyllobothriasis in Switzerland: molecular methods to de ne a clinical case of Diphyllobothrium infection as Diphyllobothrium dendriticum, August 2010. EuroSurveillance, 18(3): ii, 20355. Devi, C.S., Shashikala, Srinivasan, S., Murmu, U.C., Barman, P. & Kanungo, R. 2007. A rare case of diphyllobothriasis from Pondicherry, South India. Indian Journal of Medical Microbiology, 25(2): 152–154. Dorny, P., Praet, N., Deckers, N. & Gabriel, S. 2009. Emerging food-borne parasites. Veterinary Parasitology, 163(3): 196–206. Duggal, S., Mahajan, R.K., Duggal, N. & Hans, C. 2011. Case of sparganosis: a diagnostic dilemma. Indian Journal of Medical Microbiology, 29(2): 183–186. Dupouy-Camet, J. & Peduzzi, R. 2004. Current situation of human diphyllobothriasis in Europe. EuroSurveillance, 9(5): 31–35. Guo, A.J., Liu, K., Gong, W., Luo, X.N., Yan, H.B., Zhao, S.B., Hu, S.N. & Jia, W.Z. 2012. Molecular identi cation of Diphyllobothrium latum and a brief review of diphyllobothriosis in China. Acta Parasitologica, 57(3): 293–296. Jeon, H.K., Kim, K.H., Huh, S., Chai, J.Y., Min, D.Y., Rim, H.J. & Eom, K.S. 2009. Morphologic and genetic identi cation of Diphyllobothrium nihonkaiense in Korea. Korean Journal of Parasitology, 47(4): 369–375. Lee, E.B., Song, J.H., Park, N.S., Kang, B.K., Lee, H.S., Han, Y.J., Kim, H.J., Shin, E.H. & Chai, J.Y. 2007. A case of Diphyllobothrium latum infection with a brief review of diphyllobothriasis in the Republic of Korea. Korean Journal of Parasitology, 45(3): 219–223. Lou, H.Y., Tsai, P.C., Chang, C.C., Lin, Y.H., Liao, C.W., Kao, T.C., Lin, H.C., Lee, W.C. & Fan, C.K. 2007. A case of human diphyllobothriasis in northern Taiwan a er eating raw sh llets. Journal of Microbiology, Immunology and Infection, 40(5): 452–456. Lumbreras, H., Terashima, A., Alvarez, H., Tello, R. & Guerra, H. 1982. Single dose treatment with praziquantel (Cesol R, EmBay 8440) of human cestodiasis caused by Diphyllobothrium paci cum. Tropenmedizin und Parasitologie, 33(12): 5–7. ANNEX 7 SPECIFIC INFORMATION FOR THE RANKED PARASITES

Margolis, L., Rausch, R.L. & Robertson, E. 1973. Diphyllobothrium ursi from man in British Columbia – rst report of this tapeworm in Canada. Canadian Journal of Public Health, 64(6): 588–589. Mercado, R., Yamasaki, H., Kato, M., Munoz, V., Sagua, H., Torres, P. & Castillo, D. 2010. Molecular identi cation of the Diphyllobothrium species causing diphyllobothriasis in Chilean patients. Parasitology Research, 106(4): 995–1000. Navarrete, N. & Torres, P. 1994. [Prevalence of infection by intestinal helminths and protozoa in school children from a coastal locality in the province of Valdivia, Chile] [Article in Spanish]. Boletín Chileno de Parasitología, 49(3-4): 79–80. Oshima, T. & Kliks, M. 1987. E ects of marine mammal parasites on human health. International Journal of Parasitology, 17(2): 415–421. Paugam, A., Yera, H., Poirier, P., Lebuisson, A. & Dupouy-Camet, J. 2009. [Diphyllobothrium nihonkaiense infection: a new risk in relation with the consumption of salmon] [Article in French]. Presse Med [La Presse Médicale], 38(4): 675–657. Ramana, K., Rao, S., Vinaykumar, M., Krishnappa, M., Reddy, R., Sarfaraz, M., Kondle, V., Ratnamani, M. & Rao, R. 2011. Diphyllobothriasis in a nine-year-old child in India: a case report. Journal of Medical Case Reports, 5: 332. Rohela, M., Jamaiah, I., Chan, K.W. & Yuso , W.S. 2002. Diphyllobothriasis: the rst case report from Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health, 33(2): 229–230. Rohela, M., Jamaiah, I., Goh, K.L. & Nissapatorn, V. 2006. A second case of diphyllobothriasis in Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health, 37(5): 896–898. Ruttenber, A.J., Weniger, B.G., Sorvillo, F., Murray, R.A. & Ford, S.L. 1984. Diphyllobothriasis associated with salmon consumption in Paci c coast states. American Journal of Tropical Medicine and Hygiene, 33(3): 455–459. Scholz, T., Garcia, H.H., Kuchta, R. & Wicht, B. 2009. Update on the human broad tapeworm (genus Diphyllobothrium), including clinical relevance. Clinical Microbiology Reviews, 22(1): 146–160. Semenas, L., Kreiter, A. & Urbanski, J. 2001. New cases of human diphyllobothriasis in Patagonia, Argentina. Revista de Saude Publica, 35(2): 214–216. Shimizu, H., Kawakatsu, H., Shimizu, T., Yamada, M., Tegoshi, T., Uchikawa, R. & Arizono, N. 2008. Diphyllobothriasis nihonkaiense: possibly acquired in Switzerland from imported Paci c salmon. Internal Medicine, 47(14): 1359–1362.

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Torres P., Franjola, R., Weitz, J.C., Peña, G. & Morales, E. 1993. [New records of human diphyllobothriasis in Chile (1981–1992), with a case of multiple Diphyllobothrium latum infection] [Article in Spanish]. Boletín Chileno de Parasitología, 48(3-4): 39– 43. Turgeon, E.W. 1974. Letter: Diphyllobothrium latum ( sh tapeworm) in the Sioux Lookout zone. Canadian Medical Association Journal, 111(6): 507, 509. Wicht, B., de Marval, F. & Peduzzi, R. 2007. Diphyllobothrium nihonkaiense (Yamane et al., 1986) in Switzerland: rst molecular evidence and case reports. Parasitology International, 56(3): 195–199. Wicht, B., de Marval, F., Gottstein, B. & Peduzzi, R. 2008. Imported diphyllobothriasis in Switzerland: molecular evidence of Diphyllobothrium dendriticum (Nitsch, 1824). Parasitology Research, 102(2): 201–204. Yera, H., Estran, C., Delaunay, P., Gari-Toussaint, M., Dupouy-Camet, J. & Marty, P. 2006. Putative Diphyllobothrium nihonkaiense acquired from a Paci c salmon (Oncorhynchus keta) eaten in France; genomic identi cation and case report. Parasitology International, 55(1): 45–49.

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A7.7 ECHINOCOCCUS GRANULOSUS General information Echinococcus granulosus is a small (3–7 mm) cestode (tapeworm) belonging to the Taeniidae family. It belongs to the Echinococcus genus, which includes six species. e most important species of the genus in terms of public health importance and geographical distribution are E. granulosus, which causes cystic echinococcosis (CE) and E. multilocularis, which causes alveolar echinococcosis (AE). Echinococcus species require two mammalian hosts for completion of their lifecycles (end and intermediate hosts). Tapeworm segments containing eggs (gravid proglottids) or free eggs are passed in the faeces of the de nitive host, a carnivore. e eggs are ingested by intermediate hosts (many mammalian species), in which the larval stage (metacestodes) and infectious elements (protoscoleces) develop and cause CE. e cycle is completed if an infected intermediate host is eaten by a suitable carnivore. A common source of infection for carnivores is o al from infected livestock. Infection of humans is due to accidental ingestion of E. granulosus eggs passed into the environment with faeces from de nitive hosts (dogs are the main sources). E. granulosus is maintained in domestic and wildlife reservoirs, and its transmission is in uenced by human activities, behaviour, hygiene, environmental factors and the lack of cooperation among public health, agriculture and local authorities. Eggs of E. granulosus are highly resistant to environmental conditions and can remain infective for many months (up to about 1 year in a moist environment at lower ranges of temperatures of about +4°C to +15°C). Eggs are sensitive to desiccation, and are killed within 4 days at a relative humidity of 25%, and within 1 day at 0%. Heating to 60–80°C will kill these eggs in less than 5 minutes. Most importantly, E. granulosus eggs can survive freezing temperatures (Eckert et al., 1992; Gemmell and Lawson, 1986) ere are at least ten genetic variants (G1 to G10) of E. granulosus, of which seven (sheep strain G1, Tasmanian sheep strain G2, bu alo strain G3, cattle strain G5 (E. ortleppi), camel strain G6, pig strain G7/G9 and cervid strain G8) have been shown to be infectious for humans. e strain most o en associated with human CE appears to be the common sheep strain (G1). CE is not considered to be ‘strictly’ a food-borne disease because the infection occurs by ingestion of the Echinococcus eggs via contact with contaminated soil, infected dogs, or by consumption of food (mainly vegetables) or water contaminated with infected dog faeces. Food may be an important vehicle of transmission, but it may not be the primary vehicle for transmission for these parasites.

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However, given the wide distribution and relatively high incidence and severity of CE, and since CE is one of the major contributors to the global burden of parasitic zoonoses (Torgerson and Macpherson, 2011), it is necessary to consider its foodborne route. ere are continuing challenges in diagnosing CE in di erent host species, including humans (Barnes et al., 2012). In addition, no global estimates exist to date of CE burden in humans, and the incidence data is gathered from published literature that is generally based on surgical cases. Consequently, human cases of CE are systematically underreported by healthcare systems. Serra et al. (1999) and Nazirov, Ilkhamov and Ambekov (2002) reported that up to 75% of clinicor hospital-diagnosed cases are never recorded in local or national databases or published reports. One of the major factors in uencing the prevalence of CE is close contact with untreated dogs, the habit and popular tradition of eating raw or inadequately cooked foods, and drinking water contaminated with Echinococcus eggs.

Geographical distribution E. granulosus has a worldwide geographical distribution, with endemic foci present in every continent. Its distribution and prevalence depends on the presence of large numbers of sheep, cattle, goat and camel ocks that are the intermediate hosts of the parasite, and their close contact with dogs, the main nal host, which transmit the infection to humans. At the same time, the highest prevalence of CE in human and animal hosts is found in countries of the temperate zones, including several parts of Eurasia (the Mediterranean regions, southern and central parts of Russia, central Asia, China), Australia, some parts of America (especially South America) and north and east Africa (Dakkak, 2010; Eckert et al., 2001; Grosso et al., 2012; ompson and McManus, 2002). Due to the wide geographical distribution and extent greater than previously believed, CE is currently considered an emerging or re-emerging disease (Grosso et al., 2012; ompson and MacManus, 2002; Torgerson et al., 2003). Human CE, which is the most common Echinococcus spp. infection, probably accounts for more than 95% of the estimated 3 million global cases, with human AE causing only 0.3–0.5 million cases (Zhang, Ross and McManus, 2008). e annual incidence of CE can range from less than 1 to >200 per 100 000 inhabitants in various endemic areas (Pawlowski, Eckert and Vuitton, 2001; Dakkak, 2010).

Disease e oncospheres released from ingested E. granulosus eggs enter the blood stream a er penetration of the intestinal mucosa, and are distributed to the liver and other ANNEX 7 SPECIFIC INFORMATION FOR THE RANKED PARASITES

sites, where development of cysts begins. e liver is the most common site of the echinococcal cyst (>65%), followed by the lungs (25%); the cyst is seen less frequently in the spleen, kidneys, heart, bone or central nervous system (Moro and Schantz, 2009). e cysts vary greatly in size and shape, and may be present in large numbers in one organ. e location of cysts and cyst morphology depends on host factors and on the E. granulosus strain. e incubation period ranges between 2 and 15 years in general, and clinical manifestations of CE are variable and determined by the site, size and condition of the cysts. It has been shown that rates of growth of cysts are variable, ranging from 1 to 5 cm in diameter per year (Moro and Schantz, 2009), and that the cysts of E. granulosus can grow to more than 20 cm in diameter in humans, but the clinical manifestations are generally mild and the disease remains asymptomatic for a considerable period. us, CE is a chronic cyst-forming disease characterized by long-term growth of the cysts in internal organs for several years (Spruance, 1974). e slowly growing hydatid cysts can attain a volume of several litres and contain many thousands of infectious elements (protoscoleces). Due to the slow-growing nature of the cyst, even if the infection is frequently acquired in childhood, most cases with localization of cysts in the liver and lung become symptomatic and are diagnosed in adult patients. At the same time, cysts located in the brain or eye can cause severe clinical symptoms even when small; thus, most cases of intracerebral echinococcosis are diagnosed in children (Moro and Schantz, 2009). e signs and symptoms of hepatic echinococcosis can include hepatic enlargement (with or without a palpable mass in the right upper quadrant), right epigastric pain, nausea, biliary duct obstruction and vomiting. Pulmonary involvement can produce chest pain, cough and haemoptysis. CE is rarely fatal, but occasionally death occurs because of anaphylactic shock, or cardiac tamponade (Bouraoui, Trimeche and Mahdhaoui, 2005). Rupture of the cysts and sudden release of the contents can precipitate allergic reactions and produce fever, urticaria, eosinophilia and mild to fatal anaphylactic shock, as well as cyst dissemination that results in multiple secondary echinococcosis disease. Larval growth in bones is atypical; when it occurs, invasion of marrow cavities and spongiosa is common and causes extensive erosion of the bone. e mortality rate, among surgical cases, is about 2 to 4%, and it increases considerably if surgical and medical treatment and care are inadequate (Zhang, Ross and McManus, 2008; Dakkak, 2010).

Trade relevance of cystic echinococcosis A number of scienti c publications have reported that E. granulosus might be imported either with intermediate or de nitive hosts (Boubaker et al., 2013). 90 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

is could represent a threat for those countries currently free from the parasite. erefore, consideration may need to be given to the development of tools for pre-mortem diagnosis of hydatidosis in farm animals, which could be used to minimize the risk of importation of infected livestock. ere must also be increased awareness of the possible occurrence of biological strains of the parasite that might be of greater or lower infectivity for humans. At present no data are available on the actual prevalence of E. granulosus eggs in food or in drinking water in general. Even less is known about that which is traded internationally. Greater consideration of the possible occurrence of parasite strains that might be of greater or lower infectivity for humans may be important. However, the development of speci c DNA detection techniques would provide an important diagnostic tool. Action in de nitive hosts is an e ective means to strengthen the prevention of the introduction of the disease due to importation of dogs, cats and wild carnivores. Indeed, the World Organisation for Animal Health (OIE) has issued important recommendations in this regard: “Veterinary Authorities of importing countries should require the presentation of an international veterinary certi cate attesting that the animals were treated against echinococcosis/hydatidosis prior to shipment, and OIE, 2012 . that the treatment used is recognized as being e ective”

Impact of CE on economically vulnerable populations As a cosmopolitan disease, CE represents an increasing public health and socioeconomic concern in many areas of the world ((Eckert, Conraths and Tackmann, 2000; Garippa, Varcasia and Scala, 2004), and already results in a high disease burden in underdeveloped regions of the world, including areas of North Africa, the Near East, South America, Central Asia, and China (Wang, Wang and Liu, 2008). It a ects both human and animal health and has important socio-economic consequences. However, the socio-economic impact of the disease is not fully understood in most endemic countries because it is necessary to consider not only human and animal health, but also agriculture, trade and market factors. Evaluation of the costs to national economies has been reviewed by Budke, Deplazes and Torgerson (2006). However, the true impact of CE may still be substantially under-represented. In humans, costs associated with CE have been shown to have a great impact on a ected individuals, their families, and the community as a whole (Budke, Deplazes and Torgerson, 2006; Torgerson, 2003). CE represents a substantial burden on the human population, and current estimates suggest that the disease results in the loss ANNEX 7 SPECIFIC INFORMATION FOR THE RANKED PARASITES

of 1 to 3 million disability-adjusted life years (DALYs) per annum (Torgerson and Craig, 2011). e World Health Organization (WHO) considered CE as: “… not only one of the most widespread parasitic diseases, but also one of the most costly to treat and prevent in terms of public health.” (Eckert et al., 2001). Furthermore, in most reports, between 1 and 4% of CE cases are fatal (Budke, Deplazes and Torgerson, 2006; Dakkak, 2010; Torgerson, 2003). In livestock, there is a direct cost (mainly the loss of revenue through o al condemnation) and indirect costs (reductions in the growth, fecundity and milk production of infected animals) that are included in the estimate of the total costs associated with CE. According to Benner et al. (2010), indirect losses account for almost 99% of the total cost associated with CE. Torgerson and Craig (2011) estimated that the annual cost of treating cases and economic losses to the livestock industry probably amounts to US$ 2 billion.

References Barnes, T.S., Deplazes, P., Gottstein, B., Jenkins, D.J., Mathis, A., Siles-Lucas, M., Torgerson, P.R., Ziadinov, I.D. & Heath, D. 2012. Challenges for diagnosis and control of cystic hydatid disease. Acta Tropica, 123: 1–7 Benner, C., Carabin, H., Sánchez-Serrano, L.P., Budke, C.M. & Carmena, D. 2010. Analysis of the economic impact of cystic echinococcosis in Spain. Bulletin of the World Health Organization, 88: 49–57. Boubaker, G., Macchiaroli, N., Prada L., Cucher, M.A., Rosenzvit, M.C., Ziadinov, I., Deplazes, P., Saarma, U., Babba, H., Gottstein, B. & Spiliotis, M. 2013. A Multiplex PCR for the simultaneous detection and genotyping of the Echinococcus granulosus Complex. PLoS Neglected Tropical Diseases, 7(1): e2017. Online. See doi:10.1371/journal.pntd.0002017 Bouraoui, H., Trimeche, B. & Mahdhaoui, A. 2005. Echinococcosis of the heart: clinical and echocardiographic features in 12 patients. Acta Cardiologica, 60(1): 39–41. Budke, C.M., Deplazes, P. and Torgerson, P.R. 2006. Global socioeconomic impact of cystic echinococcosis. Emerging Infectious Diseases, 12: 296–303. Dakkak, A. 2010. Echinococcosis/Hydatidosis: a severe threat in Mediterranean countries. Veterinary Parasitology, 174: 2–11. Eckert J., Conraths F.J. & Tackmann K. 2000. Echinococcosis: an emerging or re-emerging zoonosis? International Journal of Parasitology, 30(12-13): 1283–1294. Eckert, J., Kutzer, E., Romel, M., Bürger, H.J. & Körting, W. (editors). 1992. Veterinärmedizinische Parasitologie. 4th edition. Verlag Paul Parey, Berlin, Germany. 905 p.

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Eckert, J., Schantz, P.M., Gasser, R.B., Torgerson, P.R., Bessonov, A.S., Movsessian, S.O., akur, A., Grimm, F. & Nikogossian, M.A. 2001. Geographic distribution and prevalence of cystic echinococcosis. pp. 20–66, in: J. Eckert, M.A. Gemmel, F.X. Meslin and Z.S. Pawlowski (editors). WHO/OIE Manual on Echinococcus in humans and animals: A public health problem of global concern. World Health Organization, Geneva, Switzerland, and World Organization for Animal Health, Paris, France. Garippa, G., Varcasia, A. & Scala, A. 2004. Cystic echinococcosis in Italy from the 1950s to present. Parassitologia, 46(4): 387–391. Gemmell, M.A. & Lawson, J.R. 1986. Epidemiology and control of hydatid disease. pp 189–216, in: R.C.A. ompson (editor). e biology of Echinococcus and hydatid disease. Allen & Unwin, London, UK. Grosso, G., Gruttadauria, S., Biondi, A., Marventano, S., Mistretta, A., Grosso, G., Gruttadauria, S., Biondi, A., Marventano, S. & Mistretta, A. 2012. Worldwide epidemiology of liver hydatidosis including the Mediterranean area. World Journal of Gastroenterology, 18: 1425–1437. Moro, P. & Schantz, P.M. 2009. Echinococcosis: a review. International Journal of Infectious Diseases, 13(2): 125–133. Nazirov, F.G., Ilkhamov, I.L. & Ambekov, N.C. 2002. Echinococcosis in Uzbekistan: types of problems and methods to improve treatment. Medical Journal of Uzbekistan, 23: 2–5. OIE (World Organisation for Animal Health). 2012. Echinococcosis/Hydatidosis. Recommendations applicable to OIE Listed diseases and other diseases of importance to international trade. Volume 2, Chapter 8.4, art. 8.4.2, in: Terrestrial Animal Health Code. OIE, Paris, France. Pawlowski, Z., Eckert, J. & Vuitton, D. 2001. Echinococcosis in humans: clinical aspects, diagnosis and treatment. pp. 20–66, in: J. Eckert, M.A. Gemmel, F.X. Meslin and Z.S. Pawlowski (editors). WHO/OIE Manual on Echinococcus in humans and animals: A public health problem of global concern. World Health Organization, Geneva, Switzerland, and World Organization for Animal Health, Paris, France. Serra, I., Garcia, V., Pizzaro, A., Luzoro, A., Cavada, G. & Lopez, J.A. 1999. [A universal method to correct underreporting of communicable diseases. Real incidence of hydatidosis in Chile, 1985-1994] [Article in Spanish]. Revista Médica de Chile, 127(4): 485–492. Spruance, L. 1974. Latent period of 53 years in a case of hydatid cyst disease. Archives of Internal Medicine, 1: 741–742.

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ompson, R.C. & McManus, D.P. 2002. Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology, 18: 452–457. Torgerson P.R. 2003. Economic e ects of echinococcosis. Acta Tropica, 85: 113–118. Torgerson, P.R. & Craig, P. 2011. Updated global burden of cystic and alveolar echinococcosis. p. 1, in: Report of the WHO Informal Working Group on cystic and alveolar echinococcosis surveillance, prevention and control, with the participation of FAO and OIE, Geneva, 22–23 June 2011. Available at http://whqlibdoc.who.int/ publications/2011/9789241502924_eng.pdf Accessed 2013-06-20. Torgerson, P.R. & Macpherson, C.N. 2011. e socioeconomic burden of parasitic zoonoses: global trends. Veterinary Parasitology, 182: 79–95. Torgerson, P.R., Karaeva, R.R., Corkeri, N., Abdyjaparov, T.A., Kuttubaev, O.T. & Shaikenov, B.S. 2003. Human cystic echinococcosis in Kyrgystan: an epidemiological study. Acta Tropica, 85: 51–61. Wang, Z., Wang, X. & Liu, X. 2008. Echinococcosis in China, a review of the epidemiology of Echinococcus spp. Ecohealth, 5: 115–126. Zhang, W., Ross, A.G. & McManus, D.P. 2008. Mechanisms of immunity in hydatid disease: implications for vaccine development. Journal of Immunology, 181: 6679– 6685.

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A7.8 ECHINOCOCCUS MULTILOCULARIS General information e fox tapeworm, Echinococcus multilocularis (Cestoda: Cyclophyllidea: Taeniidae) is mostly associated with a sylvatic life cycle, with foxes of the genera Vulpes and Alopex usually serving as de nitive hosts, although other wild canids (e.g. raccoon dogs, wolves, coyotes) may also act as de nitive hosts. A synanthropic cycle also occurs, in which domestic dogs usually act as de nitive hosts; although domestic cats (and possibly wild felids) may serve as de nitive hosts, experimental infections suggest that cats would appear to have only a minor role in the maintenance of E. multilocularis in endemic areas, and infections in cats may be of minimal public health signi cance ( ompson et al., 2006). For both sylvatic and synanthropic cycles, various di erent genera of rodents and lagomorphs may act as intermediate hosts, being infected by ingestion of the eggs released from the tapeworms in the faeces of the de nitive hosts. e most common potential intermediate hosts include rodents in the genera Microtus, Arvicola and Ondatra, and lagomorphs in the genera Ochotona, depending on location. A number of other mammals, including humans and pigs, may also be infected with the eggs of the parasite; in humans, this may result in the disease state known as alveolar echinococcosis (AE). However, as metacestode development in these non-rodent mammals seems to be incomplete or retarded, and also as these animals are less likely to be later consumed by the de nitive hosts, they do not seem to play a role in the perpetuation of the life cycle, and they are usually referred to as aberrant or accidental intermediate hosts (Böttcher et al., 2013).

Geographical distribution Data on the prevalence of AE in humans is scattered and patchy, probably partly due to diagnostic challenges, particularly in early stages of infection. However, improved diagnostics, such as speci c serological tests in combination with imaging techniques, have increased diagnostic possibilities. In North America, only a couple of cases of human AE have been recorded, despite a high prevalence and intensity of infection in wild canids and despite some populations, such as fox and coyote trappers, being highly exposed. In 2008, the EU reported an annual incidence of 1 case per 10 million inhabitants (EFSA, 2010), whereas reports from the United States of America indicate a much lower incidence (Bristow et al., 2012). It has been suggested that this di erence in incidence may represent genetic di erences between strains of parasites, rather than di erences in exposure risks or diagnostic capabilities between populations (Davidson et al., 2012). Although E. multilocularis infections in wildlife in Europe appear to be increasing and expanding in prevalence, and the pattern of prevalence in humans

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is following the same trend (Schweiger et al., 2007), human infection nevertheless continues to be considered as rare. For example, the mean annual incidence of human cases per 100 000 population, recorded with consistent methods, more than doubled in Switzerland, from 0.10 between 1993 and 2000, to 0.26 between 2001 and 2005 (Moro and Schantz, 2009), while in Latvia and Lithuania patient numbers seem to have been rising since 2002 (Bruzinskaite et al., 2007; Keis et al., 2007), indicating emergence of this infection in some parts of Europe. Expanding fox populations associated with rabies vaccination in some areas may contribute to the spread of this infection. While E. multilocularis infection apparently does not occur in Australia, Africa, South or Central America, countries in Asia and Europe, as well as North America, remain important endemic areas. In particular, Russia and adjacent countries (Belarus, Ukraine, Moldova, Turkey, Armenia, Azerbaijan, Kazakhstan, Turkmenistan, Uzbekistan, Tajikistan, Kyrgyzstan and Mongolia), nine provinces or autonomous regions in China (Tibet, Sichuan, Inner Mongolia, Gansu, Ningxia, Qinghai, Xinjiang, Heilongjiang and Shaanxi) and the Japanese island of Hokkaido are important endemic foci (Davidson et al., 2012). Indeed, by far the largest numbers of human cases are reported from three main foci in China, with prevalences ranging from 0.2% in northwestern Xinjiang to 4% in Gansu and Northwestern Sichuan (Craig, 2006). Speci c individual villages report even higher prevalence, with 16% reported from the village of Ban Ban Wan, Gansu (Vuitton et al., 2011).

Disease Adult E. multilocularis tapeworms normally cause little harm to the de nitive host and infection is asymptomatic. In intermediate hosts, including humans, ingested eggs develop to oncospheres, which penetrate the intestinal wall and are carried via blood to the liver in particular, but also to other organs, where they form multilocular cysts causing the disease, AE. From ingestion of eggs to onset of clinical symptoms (incubation time) in people may be from months to years, or even decades, depending on the location of the cysts and their speed of growth. In the vast majority of human AE cases, metacestodes of E. multilocularis initially develop in the liver (Kern, 2010), with cysts varying from a few millimetres up to 15–20 cm or more in diameter. ese cysts can also reproduce aggressively by asexual lateral budding. is gradual invasion of adjacent tissue in a tumour-like manner is the basis for the severity of this disease. Metacestodes may also spread from the liver to other internal organs, such as the lungs, spleen, heart and kidney. Symptoms of severe hepatic dysfunction appear in the advanced clinical stage, in addition to symptoms from other a ected organs. e proportion of cases of AE that are actually food-borne is di cult to estimate, as diagnosis usually occurs long a er infection and it may be di cult to associate 96 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

an infection with a food-borne event many years previously. It should be noted that the tapeworm eggs excreted in the faeces of de nitive hosts may contaminate various types of edible plants, including fruits and vegetables, as well as drinking water. e eggs are extremely tolerant of environmental conditions, as the oncosphere membrane surrounds and protects the infective part of the egg from the environment. E. multilocularis eggs are also extremely freeze-tolerant; freezing the eggs at -20°C does not a ect their infectivity. However, the eggs are sensitive to desiccation and heat. us, although there is a large potential for food-borne infection via raw produce, it is di cult to obtain evidence for this, and consumption of raw outdoor produce did not emerge as an important risk factor for AE in a German study in which other factors had considerably higher odds ratios (Kern et al., 2004). Other reports suggest that owning pet dogs with access to the outdoors may be the highest risk factor for AE (Stehr-Green et al., 1988; Kreidl et al., 1998). Nevertheless, the severity of the chronic morbidity associated with AE, and the potential for food-borne transmission without it necessarily being recognized, means that food-borne transmission should not be dismissed. While there is negligible acute morbidity associated with AE, its chronic morbidity is severe and infection is potentially fatal. Most patients su ering from a chronic carrier status need continuous medical treatment and follow-up examinations. Surgery and various endoscopic or percutaneous interventions are required. In addition to anti-infective therapy with benzimidazoles, earlier diagnosis and long-term medical care has increased patients survival time during the last 35 years (Kern, 2010).

Trade relevance Although globalization of trade suggests that E. multilocularis could also be introduced to countries via fresh produce, particularly with respect to the longevity of the infective eggs, a risk assessment from Norway concluded that import of E. multilocularis to mainland Norway (currently E. multilocularis-free) via fresh produce is unlikely (VKM, 2012). Import of this parasite to currently E. multilocularis-free regions seems to be more likely to occur via transport in either de nitive or intermediate hosts, as has previously been documented (for example, introduction to Svalbard; Davidson et al., 2012). Di erent regions of the world have veterinary regulations for treatment of dogs, wild canids and cats to avoid the import of the infection. For example, within the EU there is a speci c regulation regarding preventive health measures for the control of E. multilocularis infection in dogs (EU, 2003). From an international perspective, the OIE terrestrial code provides recommendations for the importation of dogs, wild canids and cats from an infected country.

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Impact on economically vulnerable populations It should be noted that in communities where access to either diagnosis or prolonged (life-long) treatment, or both, is limited, then the potential impact of infection is considerable. AE is a serious public health problem mainly in the more sparsely populated regions of China (including the Tibetan plateau and Inner Mongolia) and is o en associated with pastoral minority communities. Failure to diagnose AE (or its misdiagnosis) leads to advanced disease, making treatment di cult and prognosis poor; cases studies in rural China have indicated that poor public health infrastructure may result in diagnostic and treatment challenges for AE (McManus et al., 2011). us, although the prognosis for AE is reasonable when treatment is available, the prognosis is bleak in the absence of treatment or with failure for diagnosis (Torgerson et al., 2010), and in economically vulnerable populations annual mortality may be similar to the incidence. e disease burden from AE has been compared to that of rabies (Torgerson et al., 2010), with annual AE mortality estimated as being approximately one-third of that due to rabies, which has been estimated at approximately 55 000. e authors note that, unlike with rabies, there is no vaccine for AE, and therefore although AE is rare globally, in some highly endemic communities in China (and possibly other economically vulnerable populations) it imposes high burden, and is likely to be one of the leading causes of death.

References Böttcher, D., Bangoura, B., Schmäschke, R., Müller, K., Fischer, S., Vobis, V., Meiler, H., Wolf, G., Koller, A., Kramer, S., Overho , M., Gawlowska, S. & Schoon, H.A. 2013. Diagnostics and epidemiology of alveolar echinococcosis in slaughtered pigs from large-scale husbandries in Germany. Parasitology Research, 112(2): 629–636. Bristow, B.N., Lee, S., Sha r, S., Sorvillo, F. 2012. Human echinococcosis mortality in the United States, 1990-2007. PLoS Neglected Tropical Diseases, 6(2): e1524. Online. doi: 10.1371/journal.pntd.0001524 Bruzinskaite, R., Marcinkute, A., Strupas, K., Sokolovas, V., Deplazes, P., Mathis, A., Eddi, C. & Sarkūnas, M. 2007. Alveolar echinococcosis, Lithuania. Emerging Infectious Diseases, 13(10): 1618–1619. Craig, P.S. 2006. Epidemiology of human alveolar echinococcosis in China. Parasitology International, 55: S221–S225. Davidson, R.K., Romig, T., Jenkins, E., Tryland, M. & Robertson, L.J. 2012. e impact of globalization on distribution of Echinococcus multilocularis. Trends in Parasitology, 28(6): 239–247.

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EFSA (European Food Safety Authority). 2010. e community summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA Journal, 8: 1496. EU (European Union). 2003. Commission Delegated Regulation (EU) No 1152/2011 of 14 July 2011 supplementing Regulation (EC) No 998/2003 of the European Parliament and of the Council as regards preventive health measures for the control of Echinococcus multilocularis infection in dogs (Text with EEA relevance). Available at http://eur-lex.europa.eu/LexUriServ/ LexUriServ.do?uri=OJ:L:2011:296:0006:0 012:EN:PDF Accessed 2013-06-20. Keiss, J., Sondore, V., Cernusenko, A., Viksna, L. & Rozentale, B. 2007. Current trends in echinococcosis in Latvia. Abstract number: 1733_48 presented at the 17th European Congress of Clinical Microbiology and Infectious Diseases, ICC, Munich, Germany, 31 March - 04 April 2007. International Journal of Antimicrobial Agents, 29(Special issue: Problem Pathogens): S122–S123. Kern, P. 2010. Clinical features and treatment of alveolar echinococcosis. Current Opinion in Infectious Diseases, 23: 505–512. Kern, P., Ammon, A., Kron, M., Sinn, G., Sander, S., Petersen, L.R., Gaus, W. & Kern, P. 2004. Risk factors for alveolar echinococcosis in humans. Emerging Infectious Diseases, 10(12): 2088–2093. Kreidl, P., Allerberger, F., Judmaier, G., Auer, H., Aspöck, H. & Hall, A.J. 1998. Domestic pets as risk factors for alveolar hydatid disease in Austria. American Journal of Epidemiology, 147(10): 978–981. McManus, D.P., Li, Z., Yang, S., Gray, D.J. & Yang, Y.R. 2011. Case studies emphasising the di culties in the diagnosis and management of alveolar echinococcosis in rural China. Parasites & Vectors, 4: Article 196. Online. DOI: 10.1186/1756-3305-4-196 Moro, P. & Schantz, P.M. 2009. Echinococcosis: a review. International Journal of Infectious Diseases, 13(2): 125–133. Schweiger, A., Ammann, R.W., Candinas, D., Clavien, P.A., Eckert, J., Gottstein, B., Halkic, N., Muellhaupt, B., Prinz, B.M., Reichen, J., Tarr, P.E., Torgerson, P.R. & Deplazes, P. 2007. Human alveolar echinococcosis a er fox population increase, Switzerland. Emerging Infectious Diseases, 13(6): 878–882 Stehr-Green, J.K., Stehr-Green, P.A., Schantz, P.M., Wilson, J.F. & Lanier, A. 1988. Risk factors for infection with Echinococcus multilocularis in Alaska. American Journal of Tropical Medicine and Hygiene, 38(2): 380–385. ompson, R.C., Kapel, C.M., Hobbs, R.P. & Deplazes, P. 2006. Comparative development of Echinococcus multilocularis in its de nitive hosts. Parasitology, 132(5): 709–716.

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Torgerson, P.R., Keller, K., Magnotta, M. & Ragland, N. 2010. e global burden of alveolar echinococcosis. PLoS Neglected Tropical Diseases, 4(6): e722. Online. doi:10.1371/journal.pntd.0000722 VKM (Vitenskapskomitteen for Mattrygghet/Norwegian Scienti c Committee for Food Safety). 2012. Assessment of risk of introduction and establishment of Echinococcus multilocularis to mainland Norway. Prepared by L. Robertson, J. Lassen, M. Tryland and R.K. Davidson. Available at http://vkm.no/dav/d35674e4f0.pdf Accessed 2013-06-20. Vuitton, D.A., Wang, Q., Zhou, H.X., Raoul, F., Knapp, J., Bresson-Hadni, S., Wen, H. & Giraudoux, P. 2011. A historical view of alveolar echinococcosis, 160 years a er the discovery of the rst case in humans: part 1. What have we learnt on the distribution of the disease and on its parasitic agent? China Medical Journal (English). 124(18): 2943–2953.

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A7.9 ENTAMOEBA HISTOLYTICA General information Entamoeba histolytica is an intestinal protozoan and causes amoebic colitis, dysentery, and extraintestinal abscesses. Amoebiasis is the second leading cause of death from protozoan disease worldwide (Haque et al., 2003; Stanley, 2003). E. histolytica has a life cycle consisting of the infectious cyst form and the trophozoite, the invasive and disease causing stage. e incidence of amoebiasis was previously overestimated as two or more morphologically indistinguishable species were thought to be responsible for disease. However, di erentiation by molecular diagnosis such as PCR (rRNA, peroxiredoxin, tRNA-linked short tandem repeats) led to the consensus that only E. histolytica (and maybe E. moshkovskii) is invasive and causes disease, whereas E. dispar is commensal and non-invasive. e current estimation of the disease burden is approximately 50 million infections, resulting in an estimated 40 000 to 110 000 deaths annually (PAHO, 1998). Infection mostly occurs by ingestion of food or water contaminated with faeces containing E. histolytica cysts. However, direct ingestion of faeces by oral and anal sex, particularly among men who have sex with men, and also by faecal smearing among persons with intellectual disabilities, are considered to be the major route of infection in industrialized countries (Weinke et al., 1990; Nozaki, 2000). Since waterborne routes are primarily important in developing countries, the exact proportion of food-borne association with amoebiasis is not known.

Geographical distribution Amoebiasis is distributed throughout the world and is a potential health risk in all countries where water and food are not adequately separated from faecal contamination. In Mexico, serological studies showed that >8% of the population had amoebiasis (Caballero-Salcedo et al., 1994). In Hue City, Viet Nam, the annual incidence of amoebic liver abscess was reported to be 21 cases per 100 000 inhabitants (Blessmann et al., 2002). In the United States of America, about three thousand cases of amoebiasis were recorded in 1993, comprising mostly immigrants from Central and South America, Asia and the Paci c Islands (MMWR, 1994). Travellers to endemic countries and regions are also at risk of amoebiasis infections. For instance, 10% of about 500 individuals with diarrhoea a er travelling to a developing country were diagnosed with amoebiasis (Jelinek et al., 1996), and 3% of about 3000 German travellers returning from the tropical regions were infected with E. histolytica (Weinke et al., 1990).

Disease Less than 10% of individuals infected with E. histolytica develop symptoms (Haque et al., 2003; Stanley, 2003; Ali and Nozaki, 2007). Clinical symptoms of amoebic colitis include bloody diarrhoea with multiple mucoid stools, abdominal pain and

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tenderness. Fulminant amoebic colitis is characterized by profuse bloody diarrhoea, fever, pronounced leucocytosis, and severe abdominal pain, and occasionally seen in individuals at risk, including pregnant women, immunocompromised individuals, including those with AIDS, diabetes or alcoholism. Amoebic liver abscess is the most common extraintestinal manifestation of an amoebic infection. Symptoms associated with amoebic liver abscess are fever, right upper quadrant pain and hepatic tenderness, and sometimes include cough, anorexia and weight loss. Pleuropulmonary amoebiasis, amoebic brain abscess and amoebic skin abscess also occasionally occur. In most cases, amoebic infection is cured by drug treatment or is self-limiting, and persistent and chronic infection does not usually occur. Protective acquired immunity against amoebiasis does not last long, particularly in children, which leads to repeated infections. e case fatality rate of amoebiasis is not well known. However, in Japan, 10 deaths were reported among the 2574 con rmed cases in 2003–2006 (IASR, 2007). e case fatality rate in developing countries may be signi cantly higher.

Trade relevance As mentioned above, attribution of food-borne association with overall incidence of amoebiasis is not very clear. As transmission occurs through consumption of fresh produce, trade involving all endemic countries and regions may have an impact on transmission of the parasite. However, amoebiasis is considered to be mostly irrelevant to international trade. It is important to improve hygiene and awareness of potential food-borne transmission in food handlers.

Impact on economically vulnerable populations Children, particularly malnourished children, are more susceptible than adults (Haque et al., 2003). Trade-associated impact to these populations is not known.

References Ali, V. & Nozaki, T. 2007. Current therapeutics, their problems, and sulfur-containingamino-acid metabolism as a novel target against infections by “amitochondriate” protozoan parasites. Clinical Microbiology Reviews, 2007, 20:164-87. Blessmann, J., Van Linh, P., Nu, P.A., i, H.D., Muller-Myhsok, B., Buss, H. & Tannich, E. 2002. Epidemiology of amebiasis in a region of high incidence of amebic liver abscess in central Vietnam. American Journal of Tropical Medicine and Hygiene, 66(5): 578–583. Caballero-Salcedo, A., Viveros-Rogel, M., Salvatierra, B., Tapia-Conyer, R., Sepulveda-Amor, J., Gutierrez, G. & Ortiz-Ortiz, L. 1994. Seroepidemiology of amebiasis in Mexico. American Journal of Tropical Medicine and Hygiene, 50(4): 412–429.

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Haque, R., Huston, C.D., Hughes, M., Houpt, E. & Petri, W.A. Jr. 2003. Amebiasis. New England Journal of Medicine, 348: 1565–1573. IASR (Infectious Agents Surveillance Reports). 2007. Amoebiasis 2003–2006. Infectious Agent Surveillance Reports, 28: 103–104. Jelinek, T., Peyerl, G., Loånscher, T. & Nothdur , H.D. 1996. Evaluation of an antigencapture enzyme immunoassay for detection of Entamoeba histolytica in stool samples. European Journal of Clinical Microbiology and Infectious Disease, 15: 752–755. MMWR (Morbidity and Mortality Weekly Report). 1994. Summary of noti able diseases, United States. Morbidity and Mortality Weekly Report, 42: 1–73. Nozaki, T. 2000. Current problems of amebiasis in Japan and recent advances in amebiasis research. Japan Journal of Infectious Disease, 53: 229–237. PAHO (Pan American Health Organization). 1998. Mexico. pp. 357–378, in: Health in the Americas. Pan American Health Organization, Washington DC, USA. Stanley, S.L. Jr. 2003. Amoebiasis. Lancet, 361(9362): 1025–1034. Weinke, T., Friedrich-Jaenicke, B., Hopp, P. & Janitschke, K. 1990. Prevalence and clinical importance of Entamoeba histolytica in two high-risk groups: travellers returning from the tropics and male homosexuals. Journal of Infectious Diseases, 161: 1029–1031.

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A7.10 FASCIOLA SPP. General information Over 80 di erent species of food-borne trematodes have been reported from human infections (Fürst, Keiser, and Utzinger. 2012; Chai, 2007). Worldwide, about 56.2 million people were infected with food-borne trematodes (including Fasciola) in 2005: 7.9 million presented severe sequelae and 7158 died (Fürst, Keiser, and Utzinger. 2012). Fasciola (Fasciolidae) is a plant-borne trematode. Two species have been found to a ect humans: Fasciola hepatica and F. gigantica. Fascioliasis is an important disease in sheep, cattle and humans and is chie y con ned to the liver, where the most important pathogenic sequelae are hepatic lesions and brosis, and chronic in ammation of the bile ducts (Mas-Coma, Esteban and Bargues, 1999; Mas-Coma, Bargues and Valero, 2005). e emergence of fascioliasis appears to be partly related to climate change, where mainly anthropogenic modi cations of the environment have increased the geographical range of intermediate hosts (aquatic snails) and livestock (WHO, 1995; Mas-Coma, Valero and Bargues, 2009). e World Health Organization includes human fascioliasis on its list of priorities among neglected tropical diseases (NTDs) (WHO, 2008)

Geographical distribution Fascioliasis is widely distributed among herbivorous animals and humans, throughout most of the world. Human fascioliasis infection estimates increased from the 2000 reported in 1990 to 17 million people in 1992, and in 51 di erent countries in 1998 (Esteban, Bargues and Mas-Coma, 1998). Fascioliasis occurs worldwide in over 50 countries, especially where sheep or cattle are reared. In general, F. hepatica is present in Europe, Africa, Asia, the Americas and Oceania, and F. gigantica is mainly distributed in Africa and Asia (WHO, 2007). Fürst, Keiser, and Utzinger (2012) reported 2 646 515 fascioliasis patients globally, including North, Central and Latin America; North and Eastern Africa; Near East; Asia; and Europe. It has been reported, in Viet Nam, that fascioliasis is an emerging problem, increasing from 12 provinces with 500 cases in 2000, to 52 provinces with over 20 000 cases in 2012 (De et al., 2003; De, Le and Waikagul, 2006; De, 2012).

Disease People usually become infected from eating raw watercress or other water plants contaminated with immature Fasciola larvae (metacercariae). On ingestion, the larval ukes migrate through the intestinal wall, into the abdominal cavity, migrate to the liver and nally into the bile ducts, where they develop into mature, egg-

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laying adult ukes (Mas-Coma, Valero and Bargues, 2009; Esteban, Bargues and Mas-Coma, 1998). Acute morbidity In the liver the most important pathogenic sequelae are hepatic lesions such as liver tumours or abscesses, and in some cases, bleeding, and the occurrence of ectopic lesions when immature ukes deviate during migration and enter into other organs (Mas-Coma, Esteban and Bargues, 1999). e major clinical symptoms are abdominal pain, fever, dyspepsia, fatty food intolerance, weight loss, digestive disorders, jaundice, allergy, enlarged liver, lithiasis of the bile duct or the gall bladder, urticaria, and respiratory symptoms. e usual signs are hepatomegaly and splenomegaly, ascites, anaemia, chest signs, jaundice, vomiting and bleeding from the bile duct (De, 2011; Chen and Mott, 1990; Esteban, Bargues and Mas-Coma, 1998). e major sub-clinical symptoms are tumours or liver abscesses detected by ultrasound, CT scans or MRI; eosinophilia; and positive ELISA test by Fasciola antigen. e pathology typically is most pronounced in the bile ducts and liver. However, fascioliasis is treatable, for example with Triclabendazole (Egaten) (WHO, 2007) (see also CDC, 2013). Chronic morbidity Chronic infection may cause expansion and thickening of the bile duct wall, and degenerative lesions in liver tissue resulting in liver cirrhosis. In some cases, parasites in the liver tissue may be calci ed or become incorporated in a granuloma (Mas-Coma, Esteban and Bargues, 1999; Esteban, Bargues and Mas-Coma, 1998). Fascioliasis patients may experience weight loss, fever, and abdominal pain, which may result in a loss of strength and physical activity; high case fatality rates are reported (Mas-Coma, Esteban and Bargues, 1999).

Trade relevance e import of domesticated livestock such as sheep, goats, oxen, zebu cattle, bu aloes, pigs, donkeys, horses, mules, yaks, camels, dromedaries, llamas and alpacas can lead to introduction of Fasciola into non-endemic areas (Mas-Coma, Esteban and Bargues, 1999;; Mas-Coma, Bargues and Valero, 2005). Because of this, export activity may be negatively a ected, but there are no international restrictions known.

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countries. Farm income can be a ected because of direct e ects on animal health and on economic value of livestock and their products. It is important to recognize that because of climate change the distribution of vector snails, reservoir hosts and suitable ecological habitats may increase, thereby leading to greater public health problems and economic impact on livestock producers and their communities. Increasing parasite resistance to the most e ective drug, Triclabendazole, may also exacerbate these impacts.

References CDC (Centers for Disease Control). 2013. Fact sheet: Parasites - Fascioliasis (Fasciola infection). Web page. Available at http://www.cdc.gov/parasites/fasciola/index. html Accessed 2013-06-23. Chai, J.-Y. 2007. Intestinal ukes. pp. 53–115, in: K.D. Murrell and B. Fried (editors). World Class Parasites. Vol. 11. Springer, Dordrecht, e Netherlands. Chen, M.G. & Mott, K.E. 1990. Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. Tropical Diseases Bulletin, 87: R1– R38. De, N.V. 2011. Fascioliasis infection in tumour liver patients in Hanoi hospitals 2006– 2010. Tropical Medicine and International Health, 16: 274. De, N.V. 2012. An update on the parasitic diseases in Vietnam. pp. 9–21, in: International Scienti c Proceeding of Mekong-Sante-110, 10–12 May 2012, Hanoi Medical University, Viet Nam. De, N.V., Le, T.H. & Waikagul, J. 2006. Plant-borne trematodes and fascioliasis in Vietnam. Presented at 5th Seminar on Food- and Water-borne Parasitic Zoonoses (5th FBPZ), 28–30 November 2006, Bangkok, ailand. De, N.V., Murrell, K.D., Cong, le D., Cam, P.D., Chau, le V., Toan, N.D. & Dalsgaard, A. 2003. e food-borne trematode zoonoses of Vietnam. Southeast Asian Journal of Tropical Medicine and Public Health, 34(Suppl. 1): 12–34. Esteban, J.G., Bargues, M.D. & Mas-Coma, S. 1998. Geographical distribution, diagnosis and treatment of human fascioliasis: a review. Research and Reviews in Parasitology, 58: 13–42. Fürst, T., Keiser, J. & Utzinger, J. 2012. Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infectious Diseases, 12(3): 210– 221.

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Mas-Coma, S. 2004. Human fascioliasis: Epidemiological patterns in human endemic areas of South America, Africa and Asia. Southeast Asian Journal of Tropical Medicine and Public Health, 35(Suppl. 1): 1–11. Mas-Coma, S. & Bargues, M.D. 1999. Human liver ukes: a review. pp. 411–434, in: J.P. Dalton (editor). Research Reviews in Parasitology. CAB International Publishing, Wallingford, UK. Mas-Coma, S., Bargues, M.D. & Valero, M.A. 2005. Fascioliasis and other plant-borne trematode zoonoses. International Journal of Parasitology, 35(11-12): 1255–1278. Mas-Coma, M.S., Esteban, J.G. & Bargues, M.D. 1999. Epidemiology of human fascioliasis: a review and proposed new classi cation. Bulletin of the World Health Organization, 77(4): 340–346. Mas-Coma, S., Valero, M.A. & Bargues, M.D. 2009. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology, 69: 41–146. WHO (World Health Organization). 1995. Control of food-borne trematode infections. WHO Technical Reports Series, No. 849. 157 p. WHO. 2007. Report of the WHO Informal Meeting on use of triclabendazole in fascioliasis control. Geneva, Switzerland, 17–18 October 2006. Available at http:// www.who.int/neglected_diseases/ preventive_chemotherapy/WHO_CDS_NTD_ PCT_2007.1.pdf Accessed 2013-06-21. WHO. 2008. Fact sheet on fascioliasis. Action Against Worms, WHO, Geneva, Switzerland.

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A7.11 GIARDIA DUODENALIS General information Giardia duodenalis, Giardia intestinalis, and Giardia lamblia are the names used to refer to the same agellated, binucleated protozoan, but opinions di er regarding the name G. intestinalis. Recently, numerous biological and genetic analyses have shown that the same Giardia species present in humans are also found in a range of other mammalian species, so there is no taxonomic basis for the use of the name G. lamblia. For purposes of consistency we will use G. duodenalis. e protozoan G. duodenalis is the most frequent intestinal parasite for humans in many countries [1]. Although G. duodenalis is the only species found in humans and many other mammals, including pets and livestock, it is now considered a multispecies complex whose members can be assigned to at least seven distinct assemblages or groups of strains (Feng and Xiao, 2011; Cacciò and Ryan, 2008). Only assemblages A and B have been detected in humans and in a wide range of other mammalian hosts, whereas the remaining assemblages, C to H, are likely to be host speci c and have not yet been described infecting humans. One sub-assemblage of the A assemblage, the AII, has been described as infecting only humans (Feng and Xiao, 2011; Cacciò and Ryan, 2008).

Geographical distribution G. duodenalis has a global distribution, causing an estimated 8×108 cases per year, and is the most common intestinal parasite of humans in many countries. In Asia, Africa and Latin America, about 200 million people have symptomatic giardiasis, with some 500 000 new cases reported each year (Lal et al., 2013). Infection rates for giardiasis in humans are generally lower in developed countries. Food-borne transmission could occur through manure application to cropland; irrigation with contaminated water; and infected consumables such as meat and milk (Nash et al., 1987). Most food-borne outbreaks of giardiasis has been related to direct contamination by a food handler, but a role for zoonotic transmission is also suggested (e.g. the consumption of a Christmas pudding contaminated with rodent faeces, and tripe soup made from the o al of an infected sheep) (Nash et al., 1987). Unfortunately, no information is available on the proportion of food-borne sources for total G. duodenalis human infections (Nash et al., 1987).

Disease Severity of acute morbidity Approximately 50% of exposed individuals clear the infection without clinical symptoms, and approximately 5% to 15% of individuals shed cysts asymptomatically (Caeiro et al., 1999). e remaining 35% to 45% of individuals have symptomatic infection (Caeiro et al., 1999). Giardia causes a generally self-limited clinical

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illness characterized by diarrhoea, abdominal cramps, bloating, weight loss and malabsorption. It is not fully understood why some individuals develop clinical giardiasis while others remain asymptomatic. Host factors and strain variation of the parasite are both likely to be involved. Severity of chronic morbidity Chronic giardiasis may follow the acute phase of illness or may develop in the absence of an antecedent acute illness. Symptoms of chronic giardiasis may include loose stools but usually not diarrhoea; steatorrhoea; profound weight loss; malabsorption; or malaise. e manifestations may wax and wane over many months. Even in cases of otherwise asymptomatic infection, malabsorption of fats, sugars, carbohydrates and vitamins may occur. is can lead to hypoalbuminaemia and de ciencies of vitamin A, B12 and folate. Acquired lactose intolerance occurs in up to 40% of patients; clinically, this manifests as exacerbation in intestinal symptoms following ingestion of dairy products (Cantey et al., 2011). Recovery can take many weeks, even a er clearance of the parasite (Cantey et al., 2011). In some patients, persistence of infection is associated with development of malabsorption and weight loss (Ortega and Adam, 1997; Ish-Horowicz et al., 1989). Children with chronic giardiasis may present growth retardation, protuberance of the abdomen, spindly extremities, oedema and pallor. Hypochromic microcytic anaemia is common. One study among Columbian children suggested that giardiasis was a strong predictor of stunted growth (Botero-Garcés et al., 2009). Chronic illness fraction Chronic symptoms can develop in up to half of symptomatic individuals. In one study of experimentally infected individuals, 84% had a self-limited illness (mean duration 18 days); the remainder became chronically infected (Nash et al., 1987). Case fatality rates No mortality has been reported Increase in human illness potential Cultural practices and trends drive food selection and preparation, in uencing the extent of exposure to parasitic protozoa through food. In Morocco, where untreated wastewater is traditionally used for irrigation, crops were contaminated with Giardia cysts (Amahmid, Asmama and Bouhoum, 1999). Giardiasis in resident children was linked to the use of raw wastewater in agriculture (Melloul et al., 2002). In some high-income countries, the popularity of raw salads, sushi and other seafood, and of drinks prepared from imported berries, has increased the risk of food-borne cryptosporidiosis and giardiasis (Graczyk, Graczyk and Naprawska, 2011).

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Trade relevance Currently Giardia is not considered relevant for trade. However, raising awareness of potential transmission through food, implementing appropriate food safety measures, and the development of cross-border transport protocols may need to be discussed in correspondence with new knowledge and information available about this parasite and its diversity. Consequently, it can be anticipated that food groups, such as fresh fruits and vegetables, may require new food safety controls for these parasites.

Impact on economically vulnerable populations Children are more frequently infected than adults, particularly those from developing countries and those malnourished. Giardia infection in early childhood is associated with poor cognitive function and failure to thrive (Berkman et al., 2002).

References Amahmid, O., Asmama, S. & Bouhoum, K. 1999. e e ect of waste water reuse in irrigation on the contamination level of food crops by Giardia cysts and Ascaris eggs. International Journal of Food Microbiology, 49(1-2): 19–26. Berkman, D.S., Lescano, A.G., Gilman, R.H., Lopez, S. & Black, M.M. 2002. E ects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet, 359(9306): 564–571. Botero-Garcés, J.H., García-Montoya, G.M., Grisales-Patiño, D., Aguirre-Acevedo, D.C. & Alvarez-Uribe, M.C. 2009. Giardia intestinalis and nutritional status in children participating in the complementary nutrition program, Antioquia, Colombia, May to October 2006. Revista do Instituto de Medicina Tropical de São Paulo, 51(3): 155–162. Cacciò, S.M. & Ryan, U. 2008. Molecular epidemiology of giardiasis. Molecular and Biochemical Parasitology, 160(2): 75–80. Caeiro, J.P., Mathewson, J.J., Smith, M.A., Jiang, Z.D., Kaplan, M.A. & Dupont, H.L. 1999. Etiology of outpatient pediatric nondysenteric diarrhea: a multicenter study in the United States. Pediatric Infectious Disease Journal, 18(2): 94–97. Cantey, P.T., Roy, S., Lee, B., Cronquist, A., Smith, K., Liang, J. & Beach, M.J. 2011. Study of nonoutbreak giardiasis: novel ndings and implications for research. American Medical Journal, 124(12): 1175.e1-8. Online. doi: 10.1016/j.amjmed.2011.06.012. Feng, Y. & Xiao, L. 2011. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clinical Microbiology Reviews, 24(1): 110–140.

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Graczyk, Z., Graczyk, T.K. & Naprawska, A. 2011. A role of some food arthropods as vectors of human enteric infections. Central European Journal of Biology, 6(2): 145– 149. Ish-Horowicz, M., Korman, S.H., Shapiro, M., Har-Even, U., Tamir, I., Strauss, N. & Deckelbaum, R.J. 1989. Asymptomatic giardiasis in children. Pediatric Infectious Disease Journal, 8(11): 773–779. Lal, A., Baker, M.G., Hales, S. & French, N.P. 2013. Potential e ects of global environmental changes on cryptosporidiosis and giardiasis transmission. Trends in Parasitology, 29(2): 83–90 Melloul, A., Amahmid, O., Hassani, L. & Bouhoum, K. 2002. Health e ect of human wastes use in agriculture in El Azzouzia (the wastewater spreading area of Marrakesh city, Morocco). International Journal of Environmental Health Research, 12(1): 17–23. Nash, T.E., Herrington, D.A., Losonsky, G.A. & Levine, M.M. 1987. Experimental human infections with Giardia lamblia. Journal of Infectious Diseases, 156(6): 974– 984. Ortega, Y.R. & Adam, R.D. 1997. Giardia: overview and update. Clinical Infectious Diseases, 25(3): 545–549.

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A7.12 HETEROPHYIDAE AND HETEROPHYIDIASIS General information Fish-borne intestinal trematodes ( ukes), predominately the Heterophyidae, have many biological and epidemiological traits in common with the liver ukes and usually co-occur (Chai, Murrell and Lymbery, 2005). More than 35 species are reported to be zoonotic; species of Metagonimus, Haplorchis, Heterophyes and Centrocestus are the most prevalent. e number of species of sh (intermediate host) reported to be susceptible to infection with infective metacercariae is very large, more than 70, including both freshwater and marine species (Chai, 2007). An important epidemiological feature is the wide variety of reservoir hosts for these ukes, including sh-eating birds and wild and domestic mammals, especially cats, dogs and pigs. Human fondness for raw or lightly prepared sh foods is the primary human risk factor, and responsible for the wide geographical distribution of the human infections.

Geographical distribution Heterophyid infections occur worldwide because of the wide distribution of reservoir and sh host species, and risky human food behaviours that include consuming raw or lightly processed or cooked sh, especially in Asia, but also Europe, Africa, Near East, and North and South America (WHO, 1995). It has been estimated by WHO (2004) that heterophyids infect 40 to 50 million people worldwide, and that approximately 600 million are at risk for sh-borne ukes. Importantly, it is not possible to accurately determine the number of cases based on clinical and epidemiological data because of diagnostic confusion in distinguishing between heterophyid faecal eggs (the primary detection procedure) and those of the liver ukes in clinical and prevalence surveys. It is likely that under-reporting of intestinal ukes and the over-reporting of the liver ukes (commonly Clonorchis sinensis and Opisthorchis spp., especially in SE Asia and China). A second reason is that the milder clinical picture with intestinal infections may result in many “hidden infections”.

Disease Disease caused by intestinal ukes (heterophyidiasis) is generally not considered as signi cant in clinical importance as that of liver uke infections. is may not be an accurate assessment because heterophyid infections, until recently, have not been widely recognized. More recent reports demonstrate that several heterophyid species can cause signi cant pathology, although infrequently fatal, in the heart, brain and spinal cord of humans (which may be related to invasion of the circulatory system by worm eggs). Disease is usually related to worm burdens (generally true for most helminth infections in the intestine) and although many infections

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are probably sub-clinical, heavy infections are o en associated with diarrhoea, mucus-rich faeces, catarrhal in ammation, abdominal pain, dyspepsia, anorexia, nausea and vomiting, the most prominent symptoms being malabsorption and diarrhoea. A recent report on Haplorchis taichui infection in ailand revealed that mucosal ulceration, mucosal and sub-mucosal haemorrhages, fusion and shortening of villi, chronic in ammation, and brosis of the sub-mucosa can occur. Because the extent of intestinal uke infections have only recently been recognized, there is little basis on which to estimate overall health impact. Case fatality rates especially have not been estimated because disease is usually related to worm burdens and while serious in heavy infections, the majority of epidemiological data suggests most infections are moderate to light, and hence most are probably subclinical. A recent estimate of intestinal trematode infections suggested morbidity estimates for DALYs as 83 699 (Fürst, Keiser and Utzinger, 2012). However, this was based on aggregation of all intestinal ﬂuke infections, ﬁsh-borne and otherwise, and not speciﬁc to just heterophyids.

Trade relevance Importing countries apply the regulatory standards for safety and quality relevant to parasite contamination similar to that imposed for anisakids and cestodes. For example of these regulations, these are detailed in the US FDA and EC-EUFSA regulations (EU, no date; and Chapter 5 in FDA, no date).

Impact on economically vulnerable populations Impact is not easily estimated because the communities most at risk consume locally produced sh and are not commonly involved in the large-scale aquaculture that accounts for most exports of sh. However, as poverty levels are reduced in rural areas, the awareness and demand for higher quality and safer sh can be expected to rise; this could have a negative impact on sh farmers who produce for the local or national markets (WHO, 2004).

Other relevant information Because of the importance in heterophyid epidemiology of non-human reservoir hosts (e.g. sh-eating birds, dogs, cats) (Anh et al., 2009), attempts to change longentrenched food behaviours of people (i.e. consumption of raw sh) or the application of human mass drug treatment strategies are not likely to have a sustainable impact on sh infections. Instead, e orts should be made to improve sh production practices to control risk of sh infections.

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References Anh, L.T.N., Phuong, T.N., Murrell, K.D., Johansen, M.V., Dalsgaard A., u, T.L, Chi, K.T.B. & amsborg, S.M. 2009. Animal reservoir hosts and sh-borne zoonotic trematode infections on sh farms, Vietnam. Emerging Infectious Diseases, 15: 540–546. Chai, J.Y. 2007. Intestinal ukes. pp. 53–115 (Ch. 2), in: K.D. Murrell and B. Fried (editors). Food-borne Parasitic Zoonoses. Springer, New York, USA. Chai, J.Y., Murrell, K.D. & Lymbery, A. 2005. Fishborne zoonoses: status and issues. International Journal of Parasitology, 35: 1233–1254. Chai, J.Y., Murrell, K.D. & Lymbery, A.J. 2005. Fish-borne parasitic zoonoses: status and issues. International Journal for Parasitology, 35(11-12): 1233–1254.

EU (European Union). No date. EU import conditions for seafood and other shery products. Available at http://ec.europa.eu/food/international/trade/im_cond_ sh_en.pdf Accessed 2013-06-21. FDA (Federal Drug Administration). No date. Chapter 5 – Parasites, in: Fish and Fishery Products Hazards and Controls Guidance. 4th Edition, November 2011. Available at http://www.fda.gov/ downloads/Food/GuidanceRegulation/UCM252393.pdf Accessed 2013-08-24 Fürst, T., Keiser, J. & Utzinger, J. 2012. Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infectious Diseases, 12(3): 210– 221. WHO (World Health Organization). 1995. Control of food-borne trematode infections. WHO Technical Reports Series, No. 849. 157 p. WHO. 2004. Report of the Joint WHO/FAO Workshop on food-borne trematode infections in Asia. Ha Noi, Viet Nam, 26–28 November 2002. World Health Organization Regional o ce for the Western Paci c. 158 p. Available at http://whqlibdoc. who.int/wpro/2004/RS_2002_GE_40(VTN).pdf Accessed 2013-06-21.

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A7.13 OPISTHORCHIIDAE General information Opisthorchiidae is a group of sh-borne zoonotic trematodes that includes the liver ukes Opisthorchis viverrini, Clonorchis sinensis and O. felineus. e life cycle of the liver uke involves freshwater snails (Bithynia spp.) as rst intermediate hosts, cyprinid sh as second intermediate hosts, humans as the de nitive hosts, and cats and dogs as reservoir hosts. Humans are infected by consumption of undercooked sh containing viable metacercariae, and the infection induces hepatobiliary pathology that eventually leads to bile duct cancer, cholangiocarcinoma (CCA), the leading cause of death in Asia. Because of a strong link to CCA, O. viverrini and C. sinensis are known as type 1 carcinogens (IARC, 2012). It is estimated that the number of people infected with liver uke may be as many as 25 million with 10 million for O. viverrini, 15 million for C. sinensis and about 1 million for O. felineus (WHO 1995). Up to 700 million (10% of the global population) are at risk of infection when the third species, O. felineus, is considered (Keiser and Utzinger, 2005). eir contribution to the global disease burden in terms of disability-adjusted life years (DALYs) re ects substantial impact on health and well-being of the infected victims in developing countries (Fürst, Keiser and Utzinger, 2012). Infection by the liver uke causes various non-speci c gastrointestinal symptoms in some infected individuals, which are related to the intensity of infection. In C. sinensis alone, an estimated 2.5 million people may have some form of illness (Hong and Fang, 2012).

Geographical distribution (endemic regions) Human liver ukes cause public health problems in many parts of the world, particularly in Asia and Europe. C. sinensis is endemic in southern China, Korea, Taiwan, northern Viet Nam and also in Russia. O. viverrini is endemic in the Lower Mekong Basin, including ailand, Lao People’s Democratic Republic (Lao PDR), Cambodia and central Viet Nam (WHO, 1995). O. felineus is found in the former USSR and in Central Eastern Europe, and a recent review indicated that it is endemic in 13 European countries (Pozio et al., 2013).

Disease Liver uke infections primarily induce chronic in ammatory diseases of the hepatobiliary system and may subsequently cause bile duct cancer (cholangiocarcinoma). Benign hepatobiliary diseases are characterized by cholangitis, obstructive jaundice, hepatomegaly, periductal brosis, cholecystitis, and cholelithiasis. Most of these manifestations are mild and asymptomatic. However, once advanced CCA develops, clinical manifestation such as jaundice occurs in approximately half of the cases, while the other half may have no speci c symptoms.

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Severity of acute morbidity ere is little evidence of acute morbidity and it is rarely reported. is is probably due to the nature of low dose infection over many years rather than a heavy or massive infection. Acute symptoms may occur in cases with heavy infection, including epigastric pain and tenderness, fever, jaundice and diarrhoea. Severity of chronic Morbidity Chronic morbidity is more common in liver uke infections since the parasite survives more than 10 years in humans. e illness may occur in a small percentage of infected individuals and includes weakness, atulence or dyspepsia, and abdominal pain in the right upper quadrant (Upatham et al., 1984). However, preclinical hepatobiliary abnormalities can be determined by radiological examination such as ultrasonography, MRI and CT. ese include advanced periductal brosis, chronic cholecystitis, gall stones, pyogenic cholangitis, abscesses and cholangiocarcinoma. Chronic illness fraction Chronic illness occurs in a small fraction of infected people and some of the infected individuals (less than 10%) may develop severe disease and also cholangiocarcinoma (CCA). CCA is a complication of a liver uke infection (opisthorchiasis or clonorchiasis) but once it develops, it is fatal and curative treatment is not available. Unlike hepatocellular carcinoma (hepatoma), a speci c early marker or biomarker for diagnosis is not available for CCA. Several risk factors for CCA are documented and in addition to the liver uke infection by O. viverrini or C. sinensis, cholangiocarcinoma associates with other conditions such as primary schlerosing cholangitis, gall stones as well as viral hepatitis. Case fatality rates Case fatality as a result of CCA is high and in the endemic areas of opisthorchiasis, such as in northeast ailand, the district-based incidence of CCA varied from 90 to 300 per 100 000 (Sriamporn et al., 2004). Most CCA cases have poor prognosis and even with surgical treatment survival is short, depending on the stage of cancer and also the health care system. Most CCA patients survive for less than 5 years. Increase in human illness potential Generally the risk of infection is con ned to the endemic localities where active transmission occurs with ongoing transmission in human and intermediate hosts (snail and sh). However, with cross-border migration and aquaculture trading, there is a possibility that it may pose a threat outside endemic areas. Moreover, infection of the liver uke is normally contracted by ingestion of native sh species (mostly cyprinid), but aquaculture shery has been increasing and several species of cyprinid carps are cultured, and hence may have potential for transmission of the liver ukes. 116 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Trade relevance Currently, the liver uke has little trade relevance because the main sources of infection are native species of sh circulated locally in endemic countries. Aquaculture of fresh-water cyprinid or n sh (low-value aquaculture) are o en operated by small-scale farmers to serve domestic consumers. Generally, this farm practice does not meet export standards set by importing countries such as EU, Japan and United States of America, and thus may have low or little relevance for international trade. However, evidence in aquaculture in Viet Nam and China indicated potential contamination with zoonotic sh-borne trematodes, including C. sinensis in aquaculture for international trade. erefore, import of shery products from the liver uke-endemic areas, particularly Asia, may create a risk of infection to consumers. As such, prevention is required from the farm level and throughout the market chain.

Impact on economically vulnerable populations e impact on vulnerable populations in endemic areas is high. ere are potentially severe socio-economic consequences if the infected people nally develop CCA and if they are income earners in the family and community. Currently, no data on healthcare costs for CCA treatment in endemic countries (i.e. ailand and Lao PDR) are available, although it can be expected that the cost of such healthcare might be high since treatment of CCA either by surgery or palliative care is costly.

Other relevant information Concerted and comprehensive e ort is required for sustainable prevention and control of the liver ukes and is vital for reduction of CCA. Although the liver uke is recognized as one of the Neglected Tropical Diseases, the problem is di cult to solve because it links not only with public health aspects but also socio-economic and cultural dimensions. erefore, in addition to conventional chemotherapy by mass drug administration, health education, including on food safety issues, to raise awareness starting at school-age-level as well as to community members is needed for successful outcomes.

References Fürst, T., Keiser, J. & Utzinger, J. 2012. Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infectious Diseases, 12(3): 210– 221. Hong, S.T. & Fang, Y. 2012. Clonorchis sinensis and clonorchiasis: an update. Parasitology International, 61(1): 17–24.

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IARC (World Health Organization International Agency for Research On Cancer). 2012. A review of human carcinogens (6 vols). Monographs on the Evaluation of Carcinogenic Risks to Humans. IARC Monograph, 100. Keiser, J. & Utzinger, J. 2005. Emerging food-borne trematodiasis. Emerging Infectious Diseases, 11(10): 1507–1514. Pozio, E., Armignacco, O., Ferri, F. & Gomez-Morales, M.A. 2013. Opisthorchis felineus, an emerging infection in Italy and its implication for the European Union. Acta Tropica, 126(1): 54–62. Sriamporn, S., Pisani, P., Pipitgool, V., Suwanrungruang, K., Kamsa-ard, S., & Parkin, D.M. 2004. Prevalence of Opisthorchis viverrini infection and incidence of cholangiocarcinoma in Khon Kaen, northeast ailand. Tropical Medicine & International Health, 9(5): 588–594. Upatham, E.S., Viyanant, V., Kurathong, S., Rojborwonwitaya, J., Brockelman, W.Y., Ardsungnoen, S., Lee, P. & Vajrasthira, S. 1984. Relationship between prevalence and intensity of Opisthorchis viverrini infection, and clinical symptoms and signs in a rural community in northeast ailand. Bulletin of the World Health Organization, 62(3): 451–461. WHO (World Health Organization). 1995. Control of food-borne trematode infections. WHO Technical Reports Series, No. 849. 157 p.

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A7.14 PARAGONIMUS SPP. General information Paragonimiasis, also recognized as endemic haemoptysis, oriental lung uke infection, etc., is a food-borne parasitic infection caused by the lung uke of the family Paragonimidae that triggers a sub-acute to chronic in ammatory disease of the lung. Among the 30 species of trematodes ( ukes) of the genus Paragonimus that are able to infect humans and animals, the most common agent for human infection is P. westermani (John and Petri, 2006: 198). ere are about 15 species of Paragonimus known to infect humans. P. heterotremus is the aetiologic agent of human paragonimiasis in P.R. China, Lao PDR, Viet Nam and ailand. Species of Paragonimus are reported to infect humans in other places, including P. africanus in Africa and P. kellicotti in North America. P. westermani was reported for the rst time in the lungs of a human followed by recognition of the eggs in the sputum in 1880. e intermediate host and details of the parasite’s life cycle were reported between 1916 and 1922 (Manson, 1881; Cox, 2002). Paragonimus has two agents of intermediate hosts as well as humans in its life cycle. Intermediate hosts are various snails and crab species. Transmission of the parasite P. westermani to humans primarily occurs through the consumption of raw or undercooked seafood. Diagnosis is based on stool or sputum examination for the parasite’s eggs until 2 to 3 months a er infection. However, eggs are also occasionally encountered in e usion uid or biopsy material. Antibody detection is useful in light infections and in the diagnosis of extrapulmonary paragonimiasis. Praziquantel is the drug of choice, with recommended dosage of 75 mg/kg per day, divided into 3 doses over 2 days (Pachucki et al., 1984).

Geographical distribution Human paragonimiasis occurs in three endemic focal areas: Asia (P.R. China, Japan, Korea, Lao PDR, Philippines, Viet Nam, Taiwan and ailand); South and Central America (Ecuador, Peru, Costa Rica and Columbia); and Africa (Cameroon, Gambia and Nigeria) (Sripa et al., 2010). ere have been some reports of the disease in the United States of America during the past 15 years because of the increase in immigrants. Approximately 200 million people have been exposed and 20 million people have been infected worldwide with this parasite (WHO, 1995). e total number of infections can be seen in Table 1. Some detailed prevalences (Sripa et al., 2010) are: China, 4.1–5.1% in 24 provinces; Viet Nam, 0.5–15% in 10/64 provinces; ailand,

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cases reported in 23/68 provinces; Japan, cases reported with over 200 cases; Philippines, 27.2–40% in some areas; and India, endemic to northeastern states, up to 50%.

Disease Severity of acute morbidity e acute phase consists of various manifestations, including diarrhoea, abdominal pain, fever, cough, urticaria, hepatosplenomegaly, pulmonary abnormalities and eosinophilia (CDC, no date). Severity of chronic morbidity e chronic phase might embrace pulmonary manifestations such as cough, expectoration of discoloured sputum, haemoptysis and chest radiographic abnormalities. It is possible that the disease could be confused with TB. Flukes occasionally invade and reside in the pleural space without parenchymal lung involvement. Extra-pulmonary locations of the adult worms result in more severe manifestations, especially when the brain is involved. Extra-pulmonary paragonimiasis is rarely seen in humans because the worms migrate to the lungs, but cysts can develop in the brain and abdominal adhesions resulting from infection have been reported. Haemoptysis is the most common sign of the disease. Table 1 shows the number of cerebral infections in patients infected with paragonimiasis. Accordingly, the three parameters of Years Lost to Disability (YLD), Years of Life Lost (YLL) and Disbility-adjusted Life Years (DALYs) can be seen in this table which shows the importance of the disease. Chronic illness fraction No reports could be found on chronic illness cases, but column 3 in Table 1 depicts an estimation of cases that might result in chronic infection. Case fatality rates According to Table 1 and based on Global Burden of Disease (GBD) 2010 study regions, in 2005 the number of global deaths would have been 244 cases (Fürst, Keiser and Utzinger, 2012). Increase in human illness potential ere are many reports that show the increasing risk of illness potential in endemic regions. Many cases of eating roast crabs in the eld amongst schoolchildren have been reported, as well as frequent consumption of seasoned crabs by adult villagers, and papaya salad with crushed raw crab (Stanford University, no date; Song et al., 2008). In addition to this characteristic feature of the villagers’ food culture, area residents drink fresh crab juice as a traditional cure for measles, and this was also 120 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

TABLE 1 Summary of parasite-speci c and region-speci c modelled point estimates for paragonimiasis in 2005, based on Global Burden of Disease (GBD) 2010 study regions Regions Asia, east (China) Latin America, Andean (Ecuador, Peru) Asia, southeast (Laos) Asia Paci c, high income (South Korea) Global Total no. infected 22 320 640 No. of heavy infections 4 909 332 No. of cerebral infections 159 953 No. of deaths 235 YLD YLL DALYs

175 997 12 442 188 439

630 173

131 345

4420

6 960

443

7 403

203 334

43 876

1 467

780

867

957

176

23 155 105

5 084 729

165 860

244

183 738

12 972

196 710

Notes: YLD = Years Lost to Disability; YLL = Years of Life Lost; DALY = Disbility-adjusted Life Years. Source: Fürst, Keiser and Utzinger, 2012.

thought to constitute a route for infection. Kung Plah, Kung Ten (raw cray sh salad) and Nam Prik Poo (crab sauce) are popular and widely consumed dishes in ailand. Kinagang, which is semi-cooked fresh-water mountainous crabs, are eaten as an appreciated dish in the Philippines. In Viet Nam, people have the habit of eating undercooked crabs. All these data show the increasing risk of the disease in regions where eating crab is a part of the culture. When live crabs are crushed during preparation, the metacercariae may contaminate the ngers or utensils of the kitchen sta . Accidental transfer of infective cysts can occur via food preparers who handle raw seafood and subsequently contaminate cooking utensils and other foods (Yokogawa, 1965). Consumption of animals that feed on crustaceans can also transmit the parasite, such as eating raw boar meat. Food preparation techniques such as pickling and salting do not neutralize the causative agent. In some countries, crabs are soaked in wine for 3–5 minutes, and so called “drunken crabs” are eaten by people or cats and dogs; hence it is an important risk factor for transmission of the disease (Yokogawa, 1965). In the United States of America, signi cant behavioural and recreational risk factors 121

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include eating raw cray sh while on canoeing trips on local rivers, eating raw cray sh while on canoeing trips in Missouri, and eating raw cray sh while intoxicated (Diaz, 2011). In addition, raw or undercooked meat of paratenic hosts such as boar, bear, wild pig or rat, where juvenile worms can survive in the muscles for years, is also an important source of human infection. Animals such as pigs, dogs and a variety of feline species can also harbour P. westermani (CDC, No date).

Trade relevance Paragonimiasis is a neglected disease that has received relatively little attention from public health authorities. Interest in Paragonimus species outside endemic areas is increasing because of the risk of infection through consumption of crustaceans traded far from their point of origin in today’s globalized food supply. No trade limitations currently exist with regard to Paragonimus spp., but it might be of importance for the international trade of seafood from endemic areas.

Impact on economically vulnerable populations In many countries endemic for paragonimiasis, it is very di cult to change the habits of consuming raw or semi-cooked crabs and cray sh. Unfortunately, in some poor countries involved with this disease, intersectoral collaboration between governmental sectors, such as agriculture, aquaculture, public health and education and nance, is weak and this can cause an increase in the disease rate.

References CDC (Centers for Disease Control). No date. Parasites and Health: Paragonimiasis. Available at http://www.dpd.cdc.gov/DPDx/html/Frames/MR/Paragonimiasis/ body_Paragonimiasis_page2.htm Accessed 2013-06-21. Cox, F.E.G. 2002. History of human parasitology. Clinical Microbiology Reviews, 15(4): 595–612. Diaz, J.H. 2011. Boil before eating: paragonimiasis a er eating raw cray sh in the Mississippi River Basin. Journal of Louisiana State Medical Society, 163(5): 261–266. Fürst, T., Keiser, J. & Utzinger, J. 2012. Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infectious Diseases, 12(3): 210– 221. John, D.T. & Petri, W.A. (editors). 2006. Markell and Voge’s Medical Parasitology. 9th edition. Elsevier. 480 p.

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Manson, P. 1881. Distoma ringeri. Medical Times Gazette, 2: 8–9. Pachucki, C.T., Levandowski, R.A., Brown, V.A., Sonnenkalb, B.H. & Vruno, M.J. 1984. American Paragonimiasis treated with praziquantel. New England Journal of Medicine, 311: 582–583. Song, H.-Y., Min, D.-Y., Rim, H.-J., Vonghachack Youthanavanh, Bouakhasith Daluny, Vongsouvan Sengdara, Banouvong Virasack & Phommasak Bounlay. 2008. Skin test for paragonimiasis among schoolchildren and villagers in Namback District, Luangprabang Province, Lao PDR. Korean Journal of Parasitology, 46(3): 179–182. Sripa, B., Kaewkes, S., Intapan, P.M., Maleewong, W. & Brindley, P.J. 2010. Food-borne trematodiases in Southeast Asia epidemiology, pathology, clinical manifestation and control. Advances in Parasitology, 72: 305–350. Stanford University. No date [online]. Paragonimus westermani. http://www.stanford. edu/group/parasites/ParaSites2009/FatimaHassan_Paragonimus/FatimaHassan_ Paragonimus%20westermani.htm Accessed 2013-08-24. WHO (World Health Organization). 1995. Control of food-borne trematode infections. WHO Technical Reports Series, No. 849. 157 p. Yokogawa, M. 1965. Paragonimus and paragonimiasis. Advances in Parasitology, 3: 99– 158.

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A7.15 SARCOCYSTIS SPP. General information e genus Sarcocystis consists of obligate intracellular protozoan parasites with a two-host life cycle described as a prey-predator, herbivore-carnivore or intermediate-de nitive host relationship. Humans can serve as intermediate hosts for some species of Sarcocystis and as de nitive hosts for other species. Care must be taken to understand these roles and the potential sources of infection for each. In the intermediate host, sarcocysts develop in skeletal muscles, tongue, oesophagus, diaphragm and cardiac muscle, and occasionally in spinal cord and brain (Fayer, 2004a, b). Mature sarcocysts of di erent species vary in size from microscopic to macroscopic, and in the structure of the wall that surrounds 100s to 1000s of crescent-shaped bodies called bradyzoites. A er esh (meat) from the intermediate host is eaten by the carnivore de nitive host the sarcocyst wall is digested, bradyzoites are liberated and enter cells in the intestine. Each bradyzoite develops into a sexual stage and a er fertilization the oocyst stage is formed. Mature oocysts (containing two sporocysts each with four sporozoites) are excreted in the faeces and contaminate the environment. When a susceptible intermediate host ingests the oocysts in water or food they pass to the small intestine, where the sporozoites are released. Sporozoites penetrate the gut epithelium and enter endothelial cells in blood vessels throughout the body giving rise to several generations of asexual stages. e number of asexual generations and their primary sites of development di er for each species of Sarcocystis. e terminal generation of asexual development occurs in muscle cells. Maturation varies with the species and can take 2 months or more until bradyzoites form and sarcocysts become infectious for the de nitive host. Sarcocysts may persist for months or years.

Geographical distribution Sarcocystis species have been found as sarcocysts in the muscles of sh, reptiles, birds, and mammals worldwide.

Prevalence in food animals Prevalence data for all Sarcocystis infections must be interpreted carefully. ey o en re ect the ndings of physicians, public health workers, veterinarians or scientists with speci c interests. Much data are unreported and no truly large-scale population surveys have been conducted. Based on examination of tissues from abattoirs, a high percentage of cattle worldwide have been found infected with S. cruzi (infectious from cattle only to canines), the most prevalent species. Because S. hominis (infectious from cattle to humans) and S. hirsuta (infectious from cattle to felines) are di cult to distinguish except by electron microscopy, some prevalence data may be erroneous. S. hominis has not been detected in the United States

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of America, whereas up to 63% of cattle in Germany have been reported to be infected. S. suihominis (infectious from pigs to humans) was found more prevalent in Germany than Austria, but little information is available from other countries. In Brazil, all 50 samples of raw kibbe (beef) from 25 Arabian restaurants in Sao Paulo contained sarcocysts (Pena, Ogassawara and Sinhorini, 2001). Based on wall structure, S. hominis, S. hirsuta and S. cruzi were found in 94, 70 and 92% of the samples. e overall prevalence of Sarcocystis in pigs appears low, at 3–36% worldwide. S. suihominis and S. hominis have been reported in slaughtered pigs and cattle, respectively, raised in Japan (Saito et al., 1998, 1999). Although humans acquire gastrointestinal sarcocystosis by ingesting raw or undercooked meat from cattle or pigs harbouring mature cysts of S. hominis or S. suihominis, other species of meat animals that harbour Sarcocystis include sheep, goats, bison, water bu alo, yaks, a variety of wild ruminants, horses, camels, llamas and species of pigs other than the domesticated Sus scrofa (Dubey, Speer and Fayer, 1989). Many species of reptiles, birds, and mammals that harbour sarcocysts serve as food animals in various parts of the world (Dubey, Speer and Fayer, 1989).

Prevalence in humans Based on limited, somewhat focal surveys, intestinal sarcocystosis in humans was reported as more prevalent in Europe than any other continent (Dubey, Speer and Fayer, 1989). A prevalence of 10.4% of faecal specimens was found in children in Poland and 7.3% of samples from Germany. Of 1228 apprentices from the HanoiHaiphong area of Viet Nam who worked in Central Slovakia in 1987–1989, 14 (1.1%) had sporocysts of Sarcocystis spp. detected in their stool (Straka et al., 1991). Kibbe positive for S. hominis was fed to 7 human volunteers; 6 excreted sporocysts, 2 developed diarrhoea (Pena, Ogassawara and Sinhorini, 2001). A er eating raw beef, a patient in Spain with abdominal discomfort, loose stools, and sporulated oocysts in the faeces was diagnosed with S. hominis (Clavel et al., 2001). In Tibet, where Sarcocystis was detected in 42.9% of beef specimens examined from the marketplace, S. hominis and S. suihominis were found in stools from 21.8% and 0–7% of 926 persons, respectively (Yu et al., 1991). Muscular sarcocystosis in humans is rarely reported, with only about 100 cases until recently (Fayer 2004a, b). In such cases, humans harbour the sarcocyst stage and therefore serve as the intermediate host. Based on all other Sarcocystis life cycles, infected human tissues must be eaten by a carnivore to complete the life cycle. Because there is no known predatory or scavenging cycle in nature in which human tissues are eaten regularly by carnivores, humans most likely become infected accidentally by ingestion of food or water contaminated with faeces from a carnivore that participates in a primate-carnivore cycle involving an unknown

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species of Sarcocystis. Most have been from Asia and Southeast Asia, although cases from Central and South America, Africa, Europe and the United States of America have been reported (McLeod et al., 1980; Mehrotra et al., 1996). An outbreak in 7 persons of a 15 member military team occurred in Malaysia (Arness et al., 1999). During 2011, 32 patients 21–59 years of age, all residents in Europe, complained of mild to severe myalgia with onset a median of 11 days a er departing Tioman Island, Malaysia (Esposito, 2011). All cases consumed ice in beverages, 7 (70%) brushed teeth with tap water, and 6 (60%) ate fresh produce.

Disease Humans serve as de nitive hosts a er eating undercooked or raw meat containing mature cysts. S. hominis is acquired from eating beef, and S. suihominis is acquired from eating pork. e cycles must be human-cattle-human and human-pig-human. Like most other species of Sarcocystis, S. hominis and S. suihominis are genetically programmed to complete their life cycles in speci c intermediate hosts or within closely related host species. For example, sporocysts of S. hominis infect cattle and not pigs whereas those of S. suihominis infect pigs but not cattle. Human volunteers that ate raw beef containing S. hominis became infected and shed oocysts in their faeces. One person who became ill 3 to 6 hours a er eating the beef had nausea, stomach ache and diarrhoea (Aryeetey and Piekarski, 1976; Rommel and Heydorn, 1972). Other volunteers who ate raw pork containing S. suihominis had signs a er 6 to 48 hours, including bloat, nausea, loss of appetite, stomach ache, vomiting, diarrhoea, di cult breathing and rapid pulse (Rommel and Heydorn, 1972; Heydorn, 1977). Humans can also serve as intermediate hosts with asexual stages developing throughout the body and cysts forming in striated muscles. In such cases, humans apparently are accidental hosts because it is extremely rare that carnivores eat humans and unless that happens frequently a cycle cannot be maintained. Vasculitis, fever, myalgias, bronchospasm, pruritic rashes, lymphadenopathy, and subcutaneous nodules associated with eosinophilia, elevated erythrocyte sedimentation rate, and elevated creatinine kinase levels can last for weeks to several months (Fayer, 2004a, b). An American who, 4 years earlier, travelled extensively in Asia, had for over a year intermittent lesions on his arms, legs, soles of his feet, and trunk, beginning as subcutaneous masses associated with overlying erythaema (MacLeod et al., 1980).

Trade relevance Only those meat products that contain grossly visible cysts are recognized as infected. Although rarely reported in recent decades, they have been found predominantly in sheep in North America and recently in alpacas in Peru, but the 126 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

impact on trade is unknown. Eosinophilic myositis (a greenish sheen on portions of beef carcasses that resulted in condemnation of parts or entire carcasses) was once attributed solely to Sarcocystis infections, but other causes may be possible. Some countries might have import restrictions related to sarcocysts in meat, which might complicate trade in animals or meat due to the lack of diagnostic tools.

Impact on economically vulnerable populations Sarcocysts have been identi ed in carcasses of alpacas in the altiplano of Peru, which have been found un t for consumption and of no commercial value, resulting in economic loss to local farmers (Vitaliano Cama, 2013, pers. comm.). Documentation of the impact is not available.

References Arness, M.K., Brown, J.D., Dubey, J.P., Nea e, R.C. & Granstrom, D.E. 1999. An outbreak of acute eosinophilic myositis due to human Sarcocystis parasitism. American Journal of Tropical Medicine and Hygiene, 61: 548–553. Aryeetey, M.E. & Piekarski, G. 1976. Serologische Sarcocystis-studien an Menschen und Ratten. Zeitschri fur Parasitenkunde, 50: 109–124. Clavel, A., Doiz, O., Varea, M., Morales, S., Castillo, F.J., Rubio, M.C. & GomezLus, R. 2001. Molestias abdominales y heces blandas en consumidor habitual de carne de vacuno poco cocinada. Enfermedades Infecciosas y Microbiología Clínica, 19: 29–30. Dubey, J.P., Speer, C.A. & Fayer, R. 1989. Sarcocystis of animals and man. CRC Press, USA. 215 p. Esposito, D.H. 2011. Muscular sarcocystosis in travelers returning from Tioman Island, Malaysia – 2011. Presented at International Congress on Emerging Infectious Disease (Abstract). Fayer, R. 2004a. Sarcocystis of humans. In: D.S. Lindsay and L.M. Weiss (editors). Opportunistic Infections: Toxoplasma, Sarcocystis and Microsporidia. Kluwer Academic Publishers, Boston, USA. 256 p. Fayer, R. 2004b. Sarcocystis in human infections. Clinical Microbiology Reviews, 17(4): 894–902. Heydorn, A.O. 1977. Sarkosporidien en ziertes Fleisch als mogliche Krankheitsurache fur den Menschen. Archiv für Lebensmittelhygiene, 28: 27–31. McLeod, R., Hirabayashi, R.N., Rothman, W. & Remington, J.R. 1980. Necrotizing vasculitis and Sarcocystis: a cause and e ect relationship? Southern Medical Journal, 73(10): 1380–1383. 127

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Mehrotra, R., Bisht, D., Singh, P.A., Gupta, S.C. & Gupta, R.K. 1996. Diagnosis of human Sarcocystis infection from biopsies of the skeletal muscle. Pathology, 28: 281– 282. Pena, H.F., Ogassawara, S. & Sinhorini, I.L. 2001. Occurrence of cattle Sarcocystis species in raw kibbe from Arabian food establishments in the city of Sao Paolo, Brazil, and experimental transmission to humans. Journal of Parasitology, 87: 1459–1465. Rommel, M. & Heydorn, A.O. 1972. Beitrage zum Lebenszyklus der Sarkosporidien. III. Isospora hominis (Railiet und Lucet, 1891) Wenyon, 1923, eine Dauerform des Sarkosporidien des Rindes und des Schweins. Berliner und Münchener Tierärztliche Wochenschri , 85: 143–145. Saito, M., Shibata, Y., Ohno, A., Kubo, M., Shimura, K. & Itagaki, H. 1998. Sarcocystis suihominis detected for the rst time from pigs in Japan. Japan. Journal of Veterinary Medical Science, 60: 307–309. Saito, M., Shibata, Y., Kubo, M., Sakakibara, I., Yamada, A. & Itagaki, H. 1999. First isolation of Sarcocystis hominis from cattle in Japan. Japan. Journal of Veterinary Medical Science, 61: 307–309. Straka, S., Skracikova, J., Konvit, I., Szilagyiova, M. & Michal, L. 1991. Sarcocystis species in Vietnamese workers. Ceskoslovenska Epidemiologie Mikrobiologie Immunologie, 40: 204–208. Yu, S. 1991. [Field survey of Sarcocystis infection in the Tibet autonomous region] [In Chinese] Zhongguo Yi Xue Ke Xue Yuan Xue Bao, 13: 29–32.

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A7.16 SPIROMETRA SPP. General information Sparganosis is one of the rare forms of metacestode infections caused by the pseudophyllidean tapeworms of the genus Spirometra. e plerocercoid larvae of three species of Spirometra namely Spirometra mansoni (or Spirometra erinaceieuropaei), S. mansonoides and S. proliferum are implicated in human disease (Khurana et al., 2012). e adult worm inhabits the small intestine of felines, which are the usual de nitive hosts, although adult worms have also been reported in the human intestinal tract (Wang, Tang and Yang, 2012). e adult cestode worms are hermaphrodites and consist of scolex with a pair of grooves resembling lips and several proglottids. e terminal proglottid releases numerous ovoid eggs through the uterine pore. e eggs hatch in water to liberate the ciliated, free swimming larva called the coracidium. e coracidium is ingested by the freshwater crustacean Cyclops, the rst intermediate host in which the procercoid larva is formed. e procercoid larva develops into the plerocercoid larva in the second intermediate hosts, the amphibians or reptiles that acquire the infection on ingesting the infected Cyclops. Humans contract sparganosis either by drinking water containing infected copepods or by the ingestion of inadequately cooked meat of the infected amphibians or reptiles containing the plerocercoid larva. Practices such as application of frog esh or blood as poultices on open wounds can also cause sparganosis (Parija, 2011).

Geographical distribution Although cases of sparganosis has been reported sporadically from numerous countries across the world, China and a few South East Asian countries, including ailand, South Korea and Viet Nam, contribute the majority of the case load. From 1927 to 2011, more than 1000 cases of sparganosis have been reported from China (Li et al., 2011). ailand reported 52 cases in the period 1943 to 2010. e major reason for this geographical predilection is the local social and cultural practices (Anantaphruti, Nawa and Vanvanitchai, 2011). Studies from China show that around 30% of the wild frogs and 30% of the frogs sold in markets for consumption were infected with any of the three species of Spirometra. Also, faecal examination of stray dogs and cats in one of the provinces of China showed that around 20% of the stray dogs and over 30% of the stray cats had eggs of Spirometra (Cui et al., 2011). Even though the worm, its hosts and the favourable ecological setting are present, sparganosis is a rare entity in India (Saleque, Juyal and Bhatia, 1990). Only ve cases of sparganosis have been reported to date from India: two cases of cerebral

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sparganosis, two cases of visceral sparganosis and a case of ocular sparganosis. (Khurana et al., 2012; Sundaram, Prasad and Reddy, 2003; Duggal et al., 2011; Kudesia et al., 1998; Sen et al., 1989). e most probable reason for the low prevalence in India would be the absence of practices such as consumption and poulticing of frog meat.

Disease e disease in humans is due to the migration of the plerocercoid larvae from the intestine to di erent sites of the body. Most common localizations of sparganum are in the subcutaneous connective tissue and super cial skeletal muscles, where it forms nodular lesions that are usually painful and associated with pruritis (Qin, Feng and Zheng, 2011). Other manifestations include ocular, cerebral and visceral sparganosis. Ocular sparganosis clinically presents as redness and oedema of the eyelids and conjunctivas; forward displacement of the eyeball from the orbit (proptosis); subconjunctival granulomatous lesions; and migratory hyperaemic masses of the eyelid or conjunctiva (Ye et al., 2012). e clinical manifestations of cerebral sparganosis resemble that of brain tumour, with seizures, headache or focal neurological disturbances (Finsterer and Auer, 2012). Migration of the larvae to internal organs leads to visceral sparganosis. Although the preferred localizations are the intestinal wall, perirenal fat and the intestinal wall, along with its peritoneal attachments (mesentry), virtually any organ can be a ected. Sparganosis of liver, lung, pericardium, breast and scrotum have been reported (Khurana et al., 2012; Huang, Gong and Lu, 2012; Lee et al., 2011; Hong et al., 2010). Disseminated sparganosis is a rare entity caused by S. proliferum, whose sparganum is pleomorphic with irregular branches and proliferative buds that detach and migrate to di erent sites, where they repeat the process and invade other organs (Stief and Enge, 2011). While sparganosis is rarely fatal, it causes signi cant morbidity, which manifests acutely as in ocular and visceral forms, while cerebral sparganosis can result in chronic neurological sequelae (Qin, Feng and Zheng, 2011). In mainland China and Guangdong province, where most cases of the disease has been reported, sparganosis has been associated with signi cant morbidity and work absenteeism (Li et al., 2011). Treatment includes the surgical removal of worm or nodule, with or without administration of anti-parasitic agents such as pyquiton or metronidazole (Anon., 1990).

Trade relevance and impact on vulnerable populations Sparganosis is a signi cant disease of the eastern world due to the habit of eating frog meat and the usage of frog muscles as poultices. In other parts of the world it occurs as a result of drinking raw water containing infected Cyclops. As the disease 130 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

has a wide variation in clinical presentation, it is o en misdiagnosed or neglected (Cui et al., 2011). Increased public awareness about the risks associated with eating or poulticing raw frog and strengthened food safety measures are needed to control the disease transmission in endemic regions (Li et al., 2011). Export of frog meat from endemic regions to other parts of the world might be restricted due to Spirometra infections.

References Anantaphruti, M.T., Nawa, Y. & Vanvanitchai, Y. 2011. Human sparganosis in an overview. Acta Tropica, 118(3): 171–176. ailand:

Anon[ymous]. 1990. Helminthic infections. pp. 235–236, in: Review of Parasitic Zoonoses. 1st ed. A.I.T.B.S. Publishers Distributors, New Delhi, India. Cui, J., Lin, X.M., Zhang, H.W., Xu, B.L. & Wang, Z.Q. 2011. Sparganosis, Henan Province, central China. Emerging Infectious Diseases, 17(1): 146–147. Duggal, S., Mahajan, R.K., Duggal, N. & Hans, C. 2011. Case of sparganosis: a diagnostic dilemma. Indian Journal of Medical Microbiology, 29(2): 183–186. Finsterer, J. & Auer, H. 2012. Parasitoses of the human central nervous system. Journal of Helminthology, 10: 1–14. Hong, S.J., Kim, Y.M., Seo, M. & Kim, K.S. 2010. Breast and scrotal sparganosis: sonographic ndings and pathologic correlation. Journal of Ultrasound Medicine, 29(11): 1627–1633. Huang, F., Gong, H.Y. & Lu, M.H. 2012. Pulmonary sparganosis mansoni: a case report. Tropical Biomedicine, 29(2): 220–223. Khurana, S., Appannanavar, S., Bhatti, H.S. & Verma, S. 2012. Sparganosis of liver: a rare entity and review of literature. BMJ Case Reports published online 6 December 2012. doi: 10.1136/bcr-2012-006790 Kudesia, S., Indira, D.B., Sarala, D., Vani, S., Yasha, T.C., Jayakumar, P.N. & Shankar, S.K. 1998. Sparganosis of brain and spinal cord: unusual tapeworm infestation (report of two cases). Clinical Neurology and Neurosurgery, 100(2): 148–152. Lee, J.H., Kim, G.H., Kim, S.M., Lee, S.Y., Lee, W.Y., Bae, J.W., Shin, K.S., Hwang, K.K., Kim, D.W., Cho, M.C. 2011. A case of sparganosis that presented as a recurrent pericardial e usion. Korean Circulation Journal, 41(1): 38–42. Li, M.-W., Song, H.-Q., Li, C., Lin, H.-Y., Xie, W.-T., Lin, R.-Q. & Zhu, X.-Q. 2011. Sparganosis in mainland China. International Journal of Infectious Diseases, 15(3): e154–156. Online. doi: 10.1016/j.ijid.2010.10.001

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Parija, S.C. 2011. Helminthic infections. pp. 203–204, in: Textbook of Medical Parasitology. 3rd ed. All India Publishers and Distributors, New Delhi, India. Qin, Y., Feng, Y. & Zheng, L. 2011. [A case of sparganosis mansoni] [In Chinese]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi, 29(4): 246. Saleque, A., Juyal, P.D. & Bhatia, B.B. 1990. Spirometra sp. in a domestic cat in India. Veterinary Parasitology, 35(3): 273–276. Sen, D.K., Muller, R., Gupta, V.P. & Chilana, J.S. 1989. Cestode larva (Sparganum) in the anterior chamber of the eye. Tropical Geographic Medicine, 41(3): 270–273. Stief, B. & Enge, A. 2011. Proliferative peritonitis with larval and cystic parasitic stages in a dog. Veterinary Pathology, 48(4): 911–914. Sundaram, C., Prasad, V.S.S.V. & Reddy, J.J.M. 2003. Cerebral sparganosis. Journal of the Association of Physicians of India, 51: 1107–1109. Wang, H., Tang, Y. & Yang, Y. 2012. [A case of Spirometra mansoni infection with both plerocercoid larvae and adult worm] [In Chinese]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi, 30(1): 40. Ye, H., Du, Y., Liu, G., Luo, X. & Yang, H. 2012. Clinical features of 8 cases of orbital sparganosis in southern China. Canadian Journal of Ophthalmology, 47(5): 453– 457.

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A7.17 TAENIA SAGINATA General information Taenia saginata is an intestinal zoonotic cestode with humans as de nitive hosts. Formerly de ned as Cysticercus bovis, the metacestode larval stage occurs in the intermediate host (cattle) as cysts, causing T. saginata cysticercosis (Abuseir et al., 2007). Upon ingestion of these cysticerci, an adult tapeworm will develop in the host’s small intestine and will reach maturity within two to three months. An adult tapeworm can measure 3 m up to 12 m and will release gravid proglottids that contain between 30 000–50 000 eggs (Murrell et al., 2005). ese proglottids leave the host by active migration through the anus or in the stools. e eggs contain a larva (oncosphere) and are infective for the intermediate host (cattle) immediately a er release from the human host. Cattle become infected orally during grazing when the environment is contaminated with eggs shed by human faeces directly (animal care takers) or via sewage plants a er ooding or sewage sediment distributed on pastures (Cabarat, Geerts and Madeline, 2002). Eggs hatch in the intestine and the oncospheres liberated from the eggs, penetrate the intestinal wall and circulate through the lymphatic system and blood stream. Following migration in the animal’s body, the larvae will develop into cysticerci a er 8 to 10 weeks in muscle tissues, including the heart, and other predilection sites such as tongue, diaphragm and the masseter muscles (Abuseir et al., 2007). Humans acquire the infection by consumption of raw or undercooked beef containing live cysticerci of T. saginata.

Geographical distribution Globally, T. saginata is the most widely distributed human Taenia tapeworm, with an estimated 60 million human infections worldwide (Craig and Ito, 2007). Human tapeworm infections occur wherever cattle husbandry is prevalent and where human faeces are not disposed of properly. Despite this, T. saginata is also present in industrialized countries with good sanitary systems, because indirect transmission to cattle pastures via contaminated sewage sludge might also occur (Cabarat, Geerts and Madeline, 2002). (Cabarat, Geerts and Madeline, 2002) reported global human taeniasis prevalence results from the last 25 years ranging from less than 0.01 to 10% in Europe and up to 36% in Dagestan. It is unclear whether the data available re ects only T. saginata or also includes T. solium infections, since Taenia eggs of all species are morphologically alike. Not many studies have been conducted in humans in many African countries, and in many instances there is di culty in di erential diagnoses with T. solium eggs. Bovine cysticercosis occurs in most of the African countries, but the epidemiological patterns in the African countries are far from being completely understood because there is a lack of surveillance systems, with consequent unavailability of data with which to quantify the disease burden.

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In the Near East, the prevalence of human T. saginata (taeniasis) is infrequently reported, as is bovine cysticercosis from meat inspection. In Europe, every single carcass of bovines above 6 weeks of age needs to be examined for bovine cysticercosis, but this does not lead to accurate data of the prevalence in cattle due to low sensitivity of the method and poor reporting systems. In addition, no prevalence data have been reported in humans. T. saginata has a global distribution, but the number of global food-borne illnesses is still not very clear due to di culties in di erential diagnosis with other Taenia infections, the asymptomatic nature of most of the infections, and rare complications, such as bowel obstructions (Craig and Ito, 2007). ere are an estimated 12 million carriers in Africa, and an incidence up to 30% in some regions has been stated (Gracey, Collins and Huey, 1999). Based on meat inspection data in various European countries, the prevalence in cattle ranges between 0.01 and 7% (Abuseir et al., 2007), but due to the lack of sensitivity of the post-mortem meat inspection there is an underestimation of the prevalence by a factor of 5 to 50 times (Dorny et al., 2000). In conclusion, despite the global distribution of T. saginata, the real prevalence of this tapeworm in humans and in cattle is underestimated due to imperfect diagnostic testing and poor reporting systems in cattle and the asymptomatic character of the disease in humans.

Disease Patients harbouring adult T. saginata tapeworms are either asymptomatic or su er from anal pruritis and discharge faecal proglottids. In some cases there might be non-speci c symptoms like vomiting, nausea, epigastric pain, diarrhoea and weight loss. T. saginata is also a rare cause of ileus, pancreatitis, cholecystitis and cholangitis. In some endemic countries, T. saginata can cause an acute cholangitis (Uygur-Bayramiçli et al., 2012). Severity of acute morbidity Low, with most infected people asymptomatic. In some cases there is more severe illness due to epigastric fullness, nausea, diarrhoea and vomiting. Rare cases of acute cholangitis have been reported. Severity of chronic morbidity Low. Weight loss can occur. In some patients there are more severe symptoms, as T. saginata have been reported as the cause of ileus, pancreatitis, cholecystitis and cholangitis.

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Chronic illness fraction Unknown, but asymptomatic carriers are most frequent. Case fatality rate Not known, but probably non-existent. Increase in human illness Unknown.

Trade relevance In Europe, bovine carcasses require mandatory meat inspection under EC regulation No. 854/2004. In the event of positive ndings during meat inspection, positive carcasses are condemned (heavily infected) or frozen if lightly infected, to inactivate cysticerci before consumption. erefore, economic losses occur and, due to the global distribution of the parasite, might be relevant.

Impact on economically vulnerable populations e impact in terms of number of infections might be high when beef is eaten raw or undercooked. is is of particular relevance in the absence of adequate hygienic conditions and appropriate veterinary public health control measures. However, since most infections in humans are asymptomatic, the impact in terms of number of reported illnesses is rather low. e economic losses might be relevant due to carcass devaluation or condemnation in those vulnerable communities with poor hygiene when beef is traded, although data are lacking to show the relevance of this point.

References Abuseir, S., Kuhne, M., Schnieder, T., Klein, G. & Epe, C. 2007. Evaluation of a serological method for the detection of Taenia saginata cysticercosis using serum and meat juice samples. Parasitology Research, 101: 131–137. Cabarat, J., Geerts, S. & Madeline, M. 2002. e use of urban sewage sludge on pastures: the cysticercosis threat. Veterinary Research, 33: 575–597 Craig, P. & Ito, A. 2007. Intestinal parasites. Current Opinions in Infectious Diseases, 20: 524–532. Dorny, P., Vallée, I., and 19 others. 2010. Development of harmonised schemes for the monitoring and reporting of Cysticercus in animals and foodstu s in the European Union. Scienti c Report submitted to EFSA. 30 p. Available at http://www.efsa. europa.eu/en/supporting/doc/34e.pdf Accessed 2013-06-22.

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Gracey, J.F., Collins, D.S. & Huey, R. 1999. Diseases caused by helminth and arthropod parasites. pp. 243–259, 635–699, in: J.F. Gracey, D.S. Collins and R.J. Huey (Authors). Meat Hygiene. 10th edition. Saunders, UK. Murrell, K.D., Dorny, P., Flisser, A., Geerts, S., Kyvsgaard, N.C., McManus, D.P., Nash, T.E. & Pawlowski, Z.S. (Editors). 2005. WHO/FAO/OIE Guidelines for the surveillance, prevention and control of taeniosis/cysticercosis. OIE, Paris, France. 139 p. Available at http://www.oie.int/doc/ged/d11245.pdf Accessed 2013-08-24 Uygur-Bayramiçli, O., Ak, O., Dabak, R., Demirhan, G., Ozer, S. 2012. Taenia saginata a rare cause of acute cholangitis: a case report. Acta Clinica Belgia, 67(6): 436–437.

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A7.18 TAENIA SOLIUM General information on the parasite Humans are de nitive hosts of Taenia solium and will shed eggs in their stool (taeniasis). Ingestion of T. solium eggs will lead to the development of cysticerci in pigs, and also in humans (cysticercosis). Cysticerci can develop in almost any tissue, but involvement of the central nervous system, known as neurocysticercosis, is the clinically most important manifestation of the disease in humans and may lead to epilepsy and death (Sorvillo, DeGiorgio and Waterman, 2007). e presence of cysticerci in pork also makes pork unsafe for human consumption and greatly reduces its market value. Humans acquire taeniasis (adult tapeworm infection) by eating raw or undercooked pork with cysticerci, the larval form of T. solium (Sorvillo, DeGiorgio and Waterman, 2007). e cysticerci evaginate and attach to the intestinal wall of the small intestine and within approximately two months develop into adult tapeworms, which can grow to more than 3 m long (Flisser, 1994). e distal proglottids detach from the worm when their eggs are mature and pass out into the environment with the human faeces. ese eggs are infective to the same (auto-infection) or other humans as well as pigs if they are ingested following direct contact with tapeworm carriers, ingestion of infected faecal matter or from consuming water or food contaminated with human faeces (Garcia et al., 2003).

Geographical distribution T. solium cysticercosis is one of the most common parasitic diseases worldwide and the estimated prevalence is greater than 50 million people (Psarros, Zouros and Coimbra. 2003; Hawk et al., 2005). e prevalence of T. solium infection varies greatly according to the level of sanitation, pig husbandry practices and eating habits in a region. e parasite is endemic in several developing countries, including in Central and South America, sub-Saharan Africa, South East Asia and Western Paci c (Schantz, 2002). In developed countries, such as the United States of America and parts of Europe, T. solium cysticercosis is considered as an emerging disease due to increased immigration and international travel (Schantz, 2002; Pal, Carpio and Sander, 2000).

Disease Clinical manifestations of T. solium cysticercosis are related to individual di erences in the number, size, and topography of lesions, and the e ciency of the host’s immune response to the parasites (Nash and Neva, 1984). Neurocysticercosis and ophthalmic cysticercosis are associated with substantial morbidity (Garcia, Gonzalez and Gilman, 2011). Epileptic seizures are the commonest presentation of neurocysticercosis and generally represent the primary or sole manifestation of ANNEX 7 SPECIFIC INFORMATION FOR THE RANKED PARASITES

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the disease. Seizures occur in 50–80% of patients with parenchymal brain cysts or calci cations, but are less common in other forms of the disease (Schantz, Wilkins and Tsang, 1998; Chopra, Kaur and Mahajan, 1981; Del Brutto et al., 1992). Severity of acute morbidity T. solium neurocysticercosis is considered responsible for over 10% of acute case admissions to the neurological ward of countries where it is endemic (Montresor and Palmer, 2006). Severity of chronic morbidity Seizure disorders raise the risk of injuries, and in New Guinea the introduction of cysticercosis was followed by an epidemic of serious burns when convulsions caused people to fall into open cooking res (Bending and Cartford, 1983). e estimated economic consequences due to chronic disability are heavy (Flisser, 1988; Carabin et al., 2006; Praet et al., 2009). Case fatality rates Several large facility-based case series studies have reported that the number of deaths from cysticercosis is relatively low and that the case-fatality rate is <1% (Sorvillo, DeGiorgio and Waterman, 2007). Global deaths due to cysticercosis were estimated in 1990 to be 700 (Range (0 to 2800) and in 2010 1200 (Range 0 to 4300) for all ages and both sexes combined (Lozano et al., 2012). Increase in human illness potential With the introduction of pigs into rural farming communities by donor agencies in most countries in Africa and the short reproductive cycle of pigs, human infection with T. solium should be considered emergent, and is spreading rapidly in this region. Public health e orts for its control in pig and human populations are active in many countries.

Trade relevance Veterinary public health e orts for control of this parasite in pigs are active in many endemic countries. In most African countries carcasses may not be released even for domestic market unless they have been inspected or tested, or both, to ascertain the absence of infection. e challenge is in the enforcement of legislations on meat inspection in resource-poor communities rearing outdoor pigs. In non-endemic regions veterinary public health measurements are in place.

Impact on economically vulnerable populations Neurocysticercosis due to T. solium infection is one of the main causes of epilepsy in rural African communities (Pal, Carpio and Sander, 2000). is comes with 138 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

social stigma to those a ected by the parasite (Placencia et al., 1995) and the disease has substantial global impact in terms of disability adjusted life years (DALYs) and monetary losses (Carabin et al., 2006; Praet et al., 2009; Lozano et al., 2012). T. solium is considered to have economic impact when it comes to monetary loss due to carcass devaluation or condemnation (Carabin et al., 2006). e parasite has high prevalence in both pigs and humans where sanitation is poor, pigs are allowed to roam freely (free-range), or meat inspection is absent or inadequate (Garcia et al., 2003; Bern et al., 1999). ese features are mainly associated with resourcepoor communities or small-holder livestock farmers in the developing countries.

References Bending, J.J. & Catford, J.C. 1983. Epidemic of burns in New Guinea due to cerebral cysticercosis [letter]. Lancet, 1(8330): 922. Bern, C., Garcia, H.H., Evans, C., Gonzalez, A.E., Verastegui, M., Tsang, V.C.W. &. Gilman, R.H. 1999. Magnitude of the disease burden from neurocysticercosis in a developing country. Clinical Infectious Diseases, 29: 1203-9. Carabin, H., Krecek, R.C., Cowan, L.D., Michael, L., Foyaca-Sibat, H., Nash, T. & Willingham, A.L. 2006. Estimation of the cost of Taenia solium cysticercosis in Eastern Cape Province, South Africa. Tropical Medicine and International Health, 11: 906–916. Chopra, J.S., Kaur, U. & Mahajan, R.C. 1981. Cysticerciasis and epilepsy: a clinical and serological study. Transaction of Royal Society of Tropical Medicine and Hygiene, 75: 518–520. Del Brutto, O.H., Santibanez, R., Noboa, C.A., Aguirre, R., Diaz, E. & Alarcon, T.A. 1992. Epilepsy due to neurocysticercosis: analysis of 203 patients. Neurology, 42: 389–392. Flisser, A. 1988. Neurocysticercosis in Mexico. Parasitology Today, 4: 131–137. Flisser, A. 1994. Taeniasis and Cysticercosis due to Taenia solium. pp. 77–116, In: Tsieh Sun (editor). Progress in Clinical Parasitology. CRC Press, Boca Raton, FL, USA. García, H.H., Gonzalez, A.E. & Gilman, R.H. 2011. Cysticercosis of the central nervous system: how should it be managed? Current Opinion in Infectious Diseases, 24(5): 423–427. García, H.H., Gonzalez, A.E., Evans, C.A.W. & Gilman, R.H. 2003. Taenia solium cysticercosis. Lancet, 362(9383: 547–556.

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Hawk, M.W., Shahlaie, K., Kim, K.D. & eis, J.H. 2005. Neurocysticercosis: a review. Surgery and Neurology, 63: 123–132. Lozano, R., Naghavi, M., Foreman, K., Lim, S., Shibuya, K. and the Working Group. 2012. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet, 380(9859): 2095–2128. See also same authors, 2013, Lancet, 381(9867): 628–628. Montresor, A. & Palmer, K. 2006. Taeniasis/cysticercosis trend worldwide and rationale for control. Parasitology International, 55: 301–303. Nash, T.E. & Neva, F.A. 1984. Recent advances in the diagnosis and treatment of cerebral cysticercosis. New England Journal of Medicine, 311: 1492–1496. Pal, D.K., Carpio, A. & Sander, J.W. 2000. Neurocysticercosis and epilepsy in developing countries. Journal of Neurology, Neurosurgery and Psychiatry, 68: 137–143. Placencia, M., Farmer, P.J., Jumbo, L., Sander, J.W. & Shorvon, S.D. 1995. Levels of stigmatization of patients with previously untreated epilepsy in northern Ecuador. Neuroepidemiology, 14: 147–154. Praet, N., Speybroeck, N., Manzanedo, R., Berkvens, D., Nsame Nforninwe, D., Zoli, A., Quet, F., Preux, P.M., Carabin, H. & Geerts, S. 2009. e disease burden of Taenia solium cysticercosis in Cameroon. PLoS Neglected Tropical Diseases, 3(3): e406. Online. doi: 10.1371/journal.pntd.0000406. Psarros, T.G., Zouros, A. & Coimbra, C. 2003. Neurocysticercosis: a neurosurgical perspective. Southern Medical Journal, 96: 1019–1022. Schantz, P.M. 2002. Overview of global distribution and transmission. In: G. Singh and S. Prabhakar (editors). Taenia solium Cysticercosis: from basic to clinical science. CAB International, Wallingford, UK Schantz, P.M., Wilkins, P.P. & Tsang, V.C.W. 1998. Immigrants, imaging and immunoblots: the emergence of neurocysticercosis as a signi cant public health problem. pp. 213–241, in: W.M. Scheld, W.A. Craig and J.M. Hughes (editors). Emerging Infections 2. ASM Press, Washington DC, USA. Sorvillo, F.J., DeGiorgio, C. & Waterman, S.H. 2007. Deaths from Cysticercosis, United States. Emerging Infectious Diseases, 13: 230–235.

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A7.19 TOXOCARA SPP. General information Human toxocariasis is a zoonotic helminth infection caused by the migration of the larvae of Toxocara canis (mainly) and T. cati from dogs and cats respectively. Eggs of the parasite are shed in the faeces of dogs and cats, and the infective larvae then develop within the environmentally robust eggs until maturation of the infective stage larvae. Infective eggs can survive in soil for several years. Human infection primarily occurs upon ingestion of embryonated eggs. e larvae hatch in the intestine, penetrate the intestinal wall and migrate through the liver, lungs and heart, ultimately disseminating to other organs and the central nervous system (Hotez and Wilkins, 2009). e larvae do not develop further in humans, but remain under developmental arrest and can survive for many years. During their migrations they release antigens that result in systematic immune and local inammatory responses, and commonly elicit eosinophilia and immunoglobulin E antibodies. Other routes of infection include the consumption of raw vegetables grown in kitchen gardens contaminated with faeces of dogs and cats containing embryonated eggs, which may result in chronic low-dose infections. Rarely, the infection is associated with consumption of raw meat from potential paratenic hosts (in non-canid hosts, during migration, the larvae encyst in muscles and are infective), such as chicken (Nagakura et al., 1989), lamb (Salem and Schantz, 1992) or rabbit (Stürchler, Weiss and Gassner, 1990).

Geographical distribution Toxocariasis is a worldwide zoonosis (Utzinger et al., 2012). Eggs of T. canis and T. cati are found worldwide in soil that is open to contamination by dogs and cats. e eggs of these species occur in 2 to 88% of soil samples collected in various countries and regions. Seroprevalence surveys in Western countries of apparently healthy adults from urban areas indicate from 2 to 5% infection compared with 14.2–37% of adults in rural areas (Magnaval, Glickman and Dorchies, 1994a). In tropical countries the seroprevalence of Toxocara infection has been found to be higher, ranging from 63.2% (Chomel et al., 1993) to 92.8% (Magnaval et al., 1994b). e proportion of human illness attributable to a food source is very low compared with that due to contact with soil (geophagia) and the global burden of disease attributable to toxocariasis is unknown (Utzinger et al., 2012).

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Disease Toxocariasis manifests itself in three syndromes, namely visceral larval migrans (VLM), ocular larval migrans (OLM) and neurological toxocariasis. Ocular toxocariasis occurs when Toxocara larvae migrate to the eye. Symptoms and signs include vision loss, eye in ammation or damage to the retina. Typically, only one eye is a ected. It can be mistakenly diagnosed as childhood retinoblastoma, with consequent inappropriate enucleation of the eye. Visceral toxocariasis occurs when Toxocara larvae migrate to various body organs, such as the liver or central nervous system. Symptoms of visceral toxocariasis include fever, fatigue, coughing, wheezing or abdominal pain. e clinical signs of neurological toxocariasis, as with VLM, are non-speci c (Magnaval et al., 1997), leading to possible under-diagnosis of this condition. Quattrocchi et al. (2012) has shown that there is a highly signi cant association (p<0.001) between people with epilepsy and levels of antibodies to Toxocara (Odds Ratio of 1.92). In addition, there have been studies associating Toxocara infections with allergic asthma (Tonelli, 2005; Pinelli et al., 2008). Severity of acute morbidity Many people who are infected with Toxocara are asymptomatic, while others present mild or more severe symptoms a er the infection, and may develop overt ocular and visceral toxocariasis. e most severe cases are rare, but are more likely to occur in young children, who o en play in contaminated areas, or eat soil (pica) contaminated by dog or cat faeces (CDC, 2013). Severity of chronic morbidity Because of the occult nature of the infection and the non-speci city of the symptoms, the global scale of chronic morbidity is not known. Ocular toxocariasis is a particular exception to this, although prevalence appears to be relatively low and no data exists in many countries. In the United States of America between September 2009 and September 2010, 68 patients were diagnosed with ocular toxocariasis (CDC, 2011). Of these 30 had clinical data and of these 25 (83%) reported vision loss and 17 (68%) of these had permanent vision loss. VLM involving the brain is thought to be rare, but this may merely be because of under-recognition and -detection. Because toxocariasis tends to be an occult infection, the true incidence of infection and morbidity is probably greatly underestimated. Increase in human illness potential One of the main drawbacks to diagnosis of toxocariasis has been lack of diagnostic tools and clinical symptoms that are not speci c to the disease condition in humans. Considering that dogs and cats are the hosts of T. canis and T. cati, the reporting of human cases may continue to increase as diagnostic methods improve and infection in dogs (e.g. 25% (Barriga, 1988) and cats 30-60% (Petithory et al.,

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1996) remain high. In western countries, the above quoted seroprevalence surveys clearly demonstrate high infection rates, especially in children.

Trade relevance Toxocariasis may have little trade relevance at present because the main vehicle of transmission remains through raw vegetables and meats from paratenic hosts. e embryonated eggs of Toxocara canis could develop at a low threshold temperature of 11.8°C and have been shown to survive for 6 weeks between +1 and –2°C (Azam et al., 2012). e fact that the larval stages and eggs can survive under these environmental conditions and the increase in international trade of the food vehicles mentioned above would pre-empt the trade relevance for this food-borne parasite.

Impact on economically vulnerable populations e population at risk is children under 7 years with geophagic or pica characteristics. In this section of the population, infection, though rarely resulting in death, can cause untold su ering if it develops into ocular and neurological forms. e costs of treatment and chronic disabilities associated with these two forms are the major losses to a ected populations.

References Azam, D., Ukpai, O.M., Said, A., Abd-Allah, G.A. & Morgan, E.R. 2012. Temperature and the development and survival of infective Toxocara canis larvae. Parasitology Research, 110(2): 649–656. Barriga, O.O. 1988. A critical look at the importance, prevalence and control of toxocariasis and the possibilities of immunological control. Veterinary Parasitology, 29: 195–234. CDC (Centers for Disease Control). 2011. Ocular Toxocariasis – United States, 2009– 2010. Morbidity and Mortality Weekly Report, 60, No. 22. CDC. 2013. Parasites – Toxocariasis (also known as Roundworm Infection). Web page, last updated 2013-01-10. Available at http://www.cdc.gov/parasites/toxocariasis/ index.html Accessed 2013-06-23. Chomel, B.B., Kasten, R., Adams, C., Lambillotte, D., eis, J., Goldsmith, R., Koss, J., Chioino, C., Widjana, D.P. & Sutisna, P. 1993. Serosurvey of some major zoonotic infections in children and teenagers in Bali, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health, 24(2): 321–326. Hotez, P.J. & Wilkins, P.P. 2009. Toxocariasis: America’s most common neglected infection of poverty and a helminthiasis of global importance? PLoS Neglected Tropical Diseases, 3(3): e400. Online doi:10.1371/journal.pntd.0000400

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Magnaval, J.-F., Glickman, L.T. & Dorchies, P. 1994a. La toxocarose, une zoonose helminthique majeure. Revue de Medecine Veterinaire, 145(9): 611–627. Magnaval, J.-F., Michault, A., Calon, N., Charlet, J.P. 1994b. Epidemiology of human toxocariasis in La Reunion. Transaction of Royal Society of Tropical Medicine and Hygiene, 88: 531–533. Magnaval, J.-F., Galindo, V., Glickman, L.T. & Clanet, M. 1997. Human Toxocara infection of the central nervous system and neurological disorders: a case-control study. Parasitology, 115(5): 537–543. Magnaval, J.F., Glickman, L.T., Dorchies, P. & Morassin, B. 2001 Highlights of human toxocariasis. Review. Korean Journal of Parasitology, 39(1): 1–11. Nagakura, K., Tachibana, H., Kaneda, Y. & Kato, Y. 1989. Toxocariasis possibly caused by ingesting raw chicken. Journal of Infectious Diseases, 160: 735–736. Petithory, J.C., Vandemeule Broucke, E., Jousserand, P. & Bisognani, A.C. 1996. Prevalence de Toxocara cati chez le chat en France. Bulletin de la Societe Francaise de Parasitologie, 14: 179–184. Pinelli, E., Brandes, S., Dormans, J., Gremmer, E. & van Loveren, H. 2008. Infection with the roundworm Toxocara canis leads to exacerbation of experimental allergic airway in ammation. Clinical and Experimental Allergy, 38(4): 649–658. Quattrocchi, G., Nicoletti, A., Marin, B., Bruno, E., Druet-Cabanac, M. & Preux, P.M. 2012. Toxocariasis and epilepsy: systematic review and meta-analysis. PLoS Neglected Tropical Diseases, 6(8): e1775. Online. doi:10.1371/journal.pntd.0001775. Salem, G. & Schantz, P. 1992. Toxocaral visceral larva migrans a er ingestion of raw lamb liver. Clinical Infectious Diseases, 15: 743–744. Stürchler, D., Weiss, N. & Gassner, M. 1990. Transmission of toxocariasis. Journal of Infectious Diseases, 162: 571. Tonelli, E. 2005. [Toxocariasis and asthma: a relevant association] [In Portuguese]. Journal Pediatrics (Rio Janeiro). 81(2): 95–96. Utzinger, J., Becker, S.L., Knopp, S., Blum, J., Neumayr, A.L., Keiser, J. & Hatz, C.F. 2012. Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Medical Weekly, 142: w13727. Online 142:w13727. doi: 10.4414/ smw.2012.13727

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A7.20 TOXOPLASMA GONDII General Information Toxoplasma is a protozoan parasite belonging to the Phylum Apicomplexa and is infectious to practically all warm-blooded animals, including humans, livestock, birds and marine mammals. ere is only one species in the Toxoplasma genus: Toxoplasma gondii. Based on molecular analyses, in conjunction with mouse virulence information, T. gondii from Europe and North America has been classied into 3 genetic types (I, II, III), of which type I isolates are lethal to mice, irrespective of dose, while types II and III are generally avirulent for mice. In Europe, genotype II is predominant in humans and animals. Strains that did not fall into these three clonal types were previously considered atypical, but a fourth clonal type has been recently recognized, mostly in wildlife (Khan et al., 2011). In South America, particularly Brazil, a greater diversity of genotypes has been detected that also tend to be more virulent (Clementino Andrade et al., 2013; Carneiro et al., 2013), with a heavier burden of clinical disease (Dubey et al., 2012a, b). e overall life cycle of Toxoplasma contains two distinct cycles: the sexual enteroepithelial cycle and the asexual cycle. e de nitive hosts of T. gondii are members of the cat family (Felidae), thus the sexual cycle of the parasite occurs only within the intestinal epithelial cells of felids. Oocysts are the zygotic stage of the life cycle, and are excreted unsporulated in cat faeces. Speed of oocyst sporulation in the environment depends on factors such as temperature and humidity, but usually takes around three days. e oocysts are environmentally robust, and can retain infectivity in a cool damp environment for months (Guy, Dubey and Hill, 2012). e asexual cycle occurs when consumption of tissue cysts (see below) or oocysts results in infection of the intestine, and the tachyzoite form of the parasite multiplies asexually in the cells of lamina propria by repeated divisions until the cells rupture. Tachyzoites from ruptured cells are released into surrounding tissues resulting in systemic infection. Circulating tachyzoites infect new cells throughout the body, with cells in cardiac and skeletal muscle and the central nervous system more o en infected. A er several more rounds of asexual division, tissue cysts are formed and these remain intracellular. Tissue cysts of T. gondii range from 5 µm to over 100 µm in size and contain bradyzoites, which are infectious when ingested with the tissue surrounding them. If ingested by a felid, then the sexual enteroepithelial cycle occurs; if ingested by any other host, then the asexual cycle, as described in the previous paragraph occurs. Additionally, if a female host is pregnant when rst infected, then circulating tachyzoites may move through the placenta to the foetus (intrauterine or congenital transmission).

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Geographical distribution Toxoplasma gondii is perhaps the most widespread protozoan parasite a ecting humans, and it has been estimated that between 1 and 2 billion of the world’s population is infected at any one time (Montoya and Liesenfeld, 2004). It should be emphasized that the majority of these do not manifest clinical illness (see later). Infection in humans occurs worldwide, but prevalence varies signi cantly between populations. Between 11 and 40% of adults in the United States of America and UK have been found to be seropositive, but in other countries in western Europe, typical seroprevalence rates vary from 11 to 28% in Scandinavia, to 42% in Italy, and up to 67% in Belgium (Guy, Dubey and Hill, 2012). In some regions of Brazil, infection rates of over 70% have been reported, while rates of around 40% have been reported from various African countries. In Asia, infection rates vary from less than 10% to over 70% (Guy, Dubey and Hill, 2012). With the exception of congenital transmission, the majority of infections with T. gondii are considered to be food-borne, as described below, although waterborne outbreaks can also be of local importance, and water-borne infection has been suggested to be the major source of Toxoplasma infection in developing countries (Petersen, Kijlstra and Stanford, 2012). ere are three potentially infectious stages of Toxoplasma: tachyzoites, bradyzoites and oocysts, two of which (bradyzoites and oocysts) are of particular relevance to food-borne transmission. Bradyzoites may be ingested with the tissue of an infected intermediate host, while oocysts may be ingested with any produce that has the potential to be contaminated with the faeces of an infected felid. In addition, though probably of less signi cance, tachyzoites excreted in the milk might result in milk-borne infection. Outbreaks of toxoplasmosis associated with consumption of unpasteurized goats’ milk have been reported (Guy, Dubey and Hill, 2012), and consumption of such milk is considered a risk factor for T. gondii infection in the United States of America (Jones et al., 2009). Human infection via bradyzoites in meat is dependent on various factors, including prevalence of Toxoplasma infection in meat animals, cultural factors regarding meat consumption and meat preparation, and factors (such as age and immunological status) of the person exposed. Parasite factors are probably of relevance also. Virtually all edible portions of an animal can harbour viable T. gondii tissue cysts, and most species of livestock are susceptible to infection (Dubey, 2009a; Guy, Dubey and Hill, 2012). In some countries sheep and goats are the most important hosts of T. gondii, and the main source of infection to humans (Dubey, 2009b). In other countries, for example United States of America, lamb and mutton are considered relatively minor food commodities (Guy, Dubey and Hill, 2012). Of

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the major meat animal species investigated in United States of America to date, pig is the only species that has been found to frequently harbour the parasite (Dubey and Jones, 2008), although prevalence has declined in areas where they are predominantly raised indoors (Guy, Dubey and Hill, 2012). However, elevated infection in organic pigs indicates that consumption of under-cooked organic pork may represent an increasing infection route (Dubey et al., 2012a, b). e risk of acquiring toxoplasmosis from beef also demonstrates regional variability, with some European studies suggesting that it can be a signi cant contributor to human infection (Cook et al., 2000; Opsteegh et al., 2011). Although poultry are also susceptible to infection with T. gondii, and theoretically pose a source of infection to humans, the relatively limited lifespan of poultry and the fact that they tend to be well-cooked before consumption, limits their importance as sources of infection for humans (Kijlstra and Jongert, 2008). Indeed, chickens have not been indicated as a source of human infection in the United States of America, despite high infection rates in some ocks (Guy, Dubey and Hill, 2012). Game animals are also considered to be potentially important sources of meat-borne toxoplasmosis, particularly as such meat is o en consumed undercooked (Opsteegh et al., 2011), with wild boar and venison particularly implicated in Europe (Kijlstra and Jongert, 2008). In other parts of the world, other game meats may be of equal or greater importance; for example, kangaroos are considered to be highly susceptible to T. gondii infection (Kijlstra and Jongert, 2008). In Arctic regions, consumption of undercooked game meat, particularly from marine mammals, seems to be an important risk factor for human infection (Davidson et al., 2011). Human infection via oocysts occurs when a person ingests something that has been contaminated with faeces from an infected cat. As Toxoplasma oocysts are not infective at excretion, direct infection from handling an infected cat or cleaning the litter box daily is unlikely. As oocysts are very hardy (and, unlike bradyzoites, can survive freezing), contamination of produce provides a route for transmission. It is possible that the importance of the oocyst infection route has been generally under-estimated previously. In various outbreaks, as well as individual infections, use of a test detecting sporozoites has indicated that oocysts have been the source of infection rather than bradyzoites, indicating the importance of this route of infection (Boyer et al., 2012). Oocysts may also contaminate water, and can result in water-borne infections and outbreaks, or may contaminate fresh produce or other food items.

Disease e clinical picture of infection with Toxoplasma is greatly in uenced by the immune status of the infected person, and also by the virulence of the strain of parasite. In the immunocompetent, T. gondii infection is usually asymptomatic,

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but may cause a mild to moderate illness, in which typical symptoms include low grade fever, lymphadenopathy, fatigue, muscle pain, sore throat and headache. In some cases, ocular toxoplasmosis may occur, which may be accompanied by partial or total loss of vision. e rate of ocular toxoplasmosis seems to di er according to unknown factors, but is more common in South America, Central America, the Caribbean and parts of tropical Africa than in Europe and North America, and is quite rare in China (Petersen, Kijlstra and Stanford, 2012). In addition, ocular disease appears to be more severe in South America than in other continents, presumably due to the presence of extremely virulent genotypes of the parasite. Although latent Toxoplasma infection is generally accepted as being generally benign in the immunocompetent, some studies have suggested that the parasite may a ect behaviour (Flegr, 2007), perhaps being a contributory, or even causative, factor in various psychiatric disorders, including depression, anxiety and schizophrenia (Henriquez et al., 2009; Flegr, 2013). It has been proposed that Toxoplasma may a ect dopamine levels within the brain, resulting in alterations in CNS function (Flegr, 2013). Should the association between Toxoplasma infection and psychiatric dysfunction be proven, then the overall burden of disease and risk to health and well-being due to this parasite should be re-evaluated (Guy, Dubey and Hill, 2012; Flegr, 2013). In the immunocompromised and immunode cient (such as HIV-patients and those receiving profound immunosuppressive therapy), severe or life-threatening disease can result either from acute Toxoplasma infection or re-activation of a previously latent infection. Here, encephalitis is the most clinically signi cant manifestation, but retinochoroiditis, pneumonitis and other systemic disease may also occur. In patients with acquired immunode ciency syndrome (AIDS), toxoplasmic encephalitis is the most common cause of intracerebral mass lesions and ranks highly on the list of diseases resulting in the death of AIDS patients. Congenital toxoplasmosis is another serious potential manifestation of T. gondii infection; this is not food-borne infection per se, but may result from food-borne infection of the mother. In an immunocompetent mother, it is generally accepted that Toxoplasma is passed on to the foetus from an infection acquired immediately before or during pregnancy, i.e. prior to onset of the latent phase of infection. However, rare cases of transplacental infection have been reported in which the mother has had a previous latent infection. e risk of transplacental infection increases throughout pregnancy, but the risk of severe disease or foetal death decreases. Symptoms commonly associated with transplacental infection include spontaneous termination, foetal death, ventricular dilatation and intracranial calci cation (Guy, Dubey and Hill, 2012). Neonates may present with hydrocephalus,

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seizures, retinochoroiditis, spasticity, deafness, hepatosplenomegaly, jaundice or rash, and children that are asymptomatic at birth, may su er from mental retardation or retinochoroidal lesions later in life. Children who have been infected late on in the pregnancy are usually asymptomatic or have only mild complications. Again, there is variation according to strain of Toxoplasma, with more severe symptoms apparently associated with congenital toxoplasmosis in South America (Gómez-Marin et al., 2011).

Trade relevance and Impact on economically vulnerable populations As toxoplasmosis has a global distribution, the trade relevance is generally considered minimal. However, import and export of chilled (non-frozen) meat (including beef and horse) may enable spread of the di erent genotypes of Toxoplasma, with particular concern being the import of more virulent strains into new areas (Pomares et al., 2011). An elevation in vulnerable populations (e.g. immunologically compromised) who are more likely to experience clinical illness from infection with T. gondii may indicate that this parasite is of increasing importance. us, the main concerns appear to be that populations that are vulnerable to clinical toxoplasmosis may be increasing, while more virulent strains may have the potential to spread with traded produce, meat, and animals.

References Boyer, K., Hill, D., Mui, E., Wroblewski, K., Karrison, T., Dubey, J.P., Sautter, M., Noble, A.G., Withers, S., Swisher, C., Heydemann, P., Hosten, T., Babiarz, J., Lee, D., Meier, P., McLeod, R. and the Toxoplasmosis Study Group. 2011. Unrecognized ingestion of Toxoplasma gondii oocysts leads to congenital toxoplasmosis and causes epidemics in North America. Clinical and Infectious Diseases, 53(11): 1081–1089. Carneiro, A.C., Andrade, G.M., Costa, J.G., Pinheiro, B.V., Vasconcelos-Santos, D.V., Ferreira, A.M., Su, C., Januário, J.N. & Vitor, R.W. 2013. Genetic characterization of Toxoplasma gondii revealed highly diverse genotypes for isolates from newborns with congenital toxoplasmosis in south-eastern Brazil. Journal of Clinical Microbiology, 51(3): 901–907. Clementino Andrade, M.M., Pinheiro, B.V., Cunha, M.M., Carneiro, A.C., Andrade Neto, V.F. & Vitor, R.W. 2013. New genotypes of Toxoplasma gondii obtained from farm animals in northeast Brazil. Research in Veterinary Science, 94(3): 587–589.

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Cook, A.J., Gilbert, R.E., Bu olano, W., Zu erey, J., Petersen, E., Jenum, P.A., Foulon, W., Semprini, A.E. & Dunn, D.T. 2000. Sources of Toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on Congenital Toxoplasmosis. British Medical Journal, 321(7254): 142–147. Davidson, R., Simard, M., Kutz, S.J., Kapel, C.M., Hamnes, I.S. & Robertson, L.J. 2011. Arctic parasitology: why should we care? Trends in Parasitology, 27(6): 239–245. Dubey, J.P. 2009a. Toxoplasmosis of Animals and Humans. 2nd ed. CRC Press, Boca Raton, FL, USA. Dubey, J.P. 2009b. Toxoplasmosis in sheep – the last 20 years. Veterinary Parasitology, 163(1-2): 1–14. Dubey, J.P. & J.L. Jones. 2008. Toxoplasma gondii infections in humans and animals in the United States. International Journal of Parasitology, 38: 1257–1278. Dubey, J.P., Hill, D.E., Rozeboom, D.W., Rajendran, C., Choudhary, S., Ferreira, L.R., Kwok, O.C. & Su, C. 2012a. High prevalence and genotypes of Toxoplasma gondii isolated from organic pigs in northern United States of America. Veterinary Parasitology, 188(1-2): 14–18. Dubey, J.P., Lago, E.G., Gennari, S.M., Su, C. & Jones, J.L. 2012b. Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology, 139(11):1375-424. Flegr, J. 2007. E ects of Toxoplasma on human behaviour. Schizophrenia Bulletin, 33(3): 757–760. Flegr, J. 2013. How and why Toxoplasma makes us crazy. Trends in Parasitology, 29(4): 156–163. Gómez-Marin, J.E., de la Torre, A., Angel-Muller, E. and 30 others. 2011. First Colombian multicentric newborn screening for congenital toxoplasmosis. PLoS Neglected Tropical Diseases, 5(5): e1195 Online doi: 10.1371/journal.pntd.0001195. Guy, E., Dubey, J.P. & Hill, D.E. 2012. Toxoplasma gondii. pp. 167–188 (Ch. 6), in: L.J. Robertson and H.V. Smith (editors). Food-borne Protozoan Parasites. Nova Biomedical. Henriquez,, S.A., Brett, R., Alexander, J., Pratt, J. & Roberts, C.W. 2009. Neuropsychiatric disease and Toxoplasma gondii infection. Neuroimmunomodulation, 16: 122– 133. Jones, J.L., Dargelas, V., Roberts, J., Press, C., Remington, J.S. & Montoya, J.G. 2009. Risk factors for Toxoplasma gondii infection in the United States. Clinical Infectious Diseases, 49(6): 878–884.

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Khan, A., Dubey, J.P., Su, C., Ajioka, J.W., Rosenthal, B.M. & Sibley, L.D. 2011. Genetic analyses of atypical Toxoplasma gondii strains reveal a fourth clonal lineage in North America. International Journal of Parasitology, 41: 645–655. Kijlstra, A. & Jongert, E. 2008. Control of the risk of human toxoplasmosis transmitted by meat. International Journal of Parasitology, 38(12): 1359–1370. Montoya, J. & Liesenfeld, O. 2004. Toxoplasmosis. Lancet, 363: 965–976. Opsteegh, M., Prickaerts, S., Frankena, K. & Evers, E.G. 2011. A quantitative microbial risk assessment for meat-borne Toxoplasma gondii infection in e Netherlands. International Journal of Food Microbiology, 150(2-3): 103–114. Petersen, E., Kijlstra, A. & Stanford, M. 2012 Epidemiology of ocular toxoplasmosis. Ocular Immunology and In ammation, 20(2): 68–75. Pomares, C., Ajzenberg, D., Bornard, L., Bernardin, G., Hasseine, L., Dardé, M.-L. & Marty, P. 2011, Toxoplasmosis in horse meat. 2011. Emerging Infectious Diseases, 17(7): 1327–1328.

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A7.21 TRICHINELLA SPP. OTHER THAN T. SPIRALIS General information Nematodes of the genus Trichinella are maintained in nature by sylvatic or domestic cycles. e sylvatic cycle is widespread on all continents, from frigid to torrid zones except Antarctica, and it is maintained by cannibalism and the scavenging behaviour of carnivorous and omnivorous animals. Twelve taxa are recognized in the genus Trichinella, three of them (T. pseudospiralis, T. papuae, T. zimbabwensis) are clustered in the non-encapsulated clade, and the other nine are in the encapsulated clade (T. spiralis, T. nativa, T. britovi, T. murrelli, T. nelsoni, T. patagoniensis, Trichinella T6, T8 and T9). All taxa infect mammals, while whereas, T. pseudospiralis infects also birds, and T. papuae and T. zimbabwensis infect also reptiles) (Pozio et al., 2009). Only humans show the clinical disease, trichinellosis, whereas animals are generally asymptomatic and only those experimentally infected with a huge number of larvae can develop the signs of the disease. Humans acquire the infection by the ingestion of raw or poorly cooked meat of domestic and wild swine, bears, walruses, horses, badgers, dogs, cougars, jackals and turtles. Meat and meat-derived products of all Trichinella-susceptible animals are a risk for humans if consumed raw or semi-raw (Pozio and Murrell, 2006).

Geographical distribution Trichinella parasites are widespread in all continents, except Antarctica, with varying prevalence according to the environmental conditions (low temperature and high humidity versus high temperature and low humidity), wildlife, and human behaviour. For example, the common habit of hunters to leave animal carcasses in the eld a er skinning, or removing and discarding the entrails, increases the probability of transmission to new hosts (Pozio and Murrell, 2006). T. spiralis and T. pseudospiralis are the only two species with a cosmopolitan distribution for two di erent reasons: T. spiralis has been spread in the world by humans, while T. pseudospiralis is spread by birds. All the other taxa show a well de ned distribution area: T. nativa in arctic and sub-arctic regions; T. britovi in Europe, western Asia, North and West Africa; T. murrelli in United States of America, southern Canada and northern Mexico; T. nelson in eastern and southern Africa; T. patagoniensis in South America; Trichinella T6 in arctic and sub-arctic regions of North America; Trichinella T8 in southwest Africa; and Trichinella T9 in Japan (Pozio et al., 2009). In 1998, it was estimated that the global prevalence of trichinellosis was about 11 million (Dupouy-Camet, 2000). is estimate was based on the assumption that the number of trichinellosis cases was similar to that of people a ected by taeniasis/ cysticercosis, because both diseases are transmitted through pork consumption. In

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2007, an estimate of the yearly incidence suggested around 10 000 infections. is number was estimated by aggregating the highest incidence rate reported in the countries of the world in a ten-year period (Pozio, 2007). However, because of problems related to incomplete data from some regions, and to the quality of diagnostic criteria of infection, the World Health Organization’s Food-borne Disease Burden Epidemiology Reference Group (FERG) requested a systematic review of the global incidence. e systematic review of the literature available worldwide from 1986 to 2009 founds reports of 65 818 cases and 42 deaths from 41 countries (Murrell and Pozio, 2011). Most of the infections (87%) have been documented in Europe, with about half of those being from Romania.

Disease Severity of acute morbidity In most persons, the onset of the acute stage is sudden, with general weakness, chills, headache, fever (up to 40°C), excessive sweating and tachycardia. In nearly all cases, symmetrical eyelid and periocular oedema occur, and oedema frequently a ects the entire face. e blood vessels of conjunctivae become in amed, and in some persons petechiae, intraconjunctival haemorrhages and haemorrhages of nail beds occur. ese symptoms are accompanied by eosinophilia, and usually by leucocytosis. is symptomatology is followed by pain in various muscle groups, which may restrict motility. e intensity of muscle pain re ects the severity of the disease. Pain develops in nuchal and trunk muscles, in the muscles of the upper and lower extremities, and, less frequently, in masseter muscles. Pain occurs upon movement (Pozio, Gomez Morales and Dupouy-Camet, 2003). Severity of chronic morbidity It is quite di cult to distinguish what may be considered as “chronic trichinellosis”. Nonetheless, there have been reports of persons who, months or even years a er the acute stage, continued to su er from chronic pain, general discomfort, tingling, numbness and excessive sweating, and who showed signs of paranoia and a syndrome of persecution. e persistence of these symptoms has been more frequently observed among persons who had su ered severe trichinellosis. Up to ten years from infection, there have been reports of impaired muscle strength, conjunctivitis, impaired coordination and the presence of IgG antibodies, and live larvae have been detected in muscles up to 39 years a er infection, yet without clinical signs or symptoms (Pozio, Gomez Morales and Dupouy-Camet, 2003). Chronic illness fraction Chronic trichinellosis is very rarely documented; however, all cases in which trichinellosis has been de ned as “chronic” have been reported in persons who had not been treated in a timely manner (i.e. early in the invasion of the muscles by larvae) (Pozio, Gomez Morales and Dupouy-Camet, 2003). ANNEX 7 SPECIFIC INFORMATION FOR THE RANKED PARASITES

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Case fatality rates In a 24-year period (1986–2009), 42 deaths were reported worldwide, of which 24 were documented in Europe (Murrell and Pozio, 2011). Increase in human illness potential Social, political and economic factors; food behaviour; increase in animal populations susceptible to Trichinella; and the common habit of hunters to leave animal carcasses in the eld a er skinning or removing and discarding the entrails, are responsible for the reemergence of trichinellosis in humans.

Trade relevance Trade was of important relevance for horse meat in the past (Liciardi et al., 2009). Game meat (mainly from wild boar and bear) illegally imported from endemic to non-endemic countries was the source of infection for hundreds of people. Since Trichinella-infected pigs are backyard or free-ranging, they are consumed at the local level and do not reach the market. Most marketed pigs are reared in high containment-level farms and consequently are Trichinella free.

Impact on economically vulnerable populations Trichinella spp. circulate at relatively high prevalence in backyard or free-ranging pigs of poor rural areas without e cient veterinary services. However, the behaviour of the human population and the environmental conditions play an important role in the circulation of these zoonotic parasites. In addition, since Trichinella spp. circulate in wildlife, the hunters, their relatives and friends consuming game meat of Trichinella-susceptible animals can be exposed to the infection regardless of their economic and social status if game is not tested by the veterinary services.

References Dupouy-Camet, J. 2000. Trichinellosis: a worldwide zoonosis. Veterinary Parasitology, 93: 191–200. Liciardi, M., Marucci, G., Addis, G., Ludovisi, A., Gomez Morales, M.A., Deiana, B., Cabaj, W. & Pozio, E. 2009. Trichinella britovi and Trichinella spiralis mixed infection in a horse from Poland. Veterinary Parasitology, 161: 345–348. Murrell, K.D. & Pozio, E. 2011. Worldwide occurrence and impact of human trichinellosis, 1986–2009. Emerging Infectious Diseases, 17: 2194–2202. Pozio, E. 2007. World distribution of Trichinella spp. infections in animals and humans. Veterinary Parasitology, 149: 3–21.

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Pozio, E., Gomez Morales, M.A. & Dupouy-Camet, J. 2003. Clinical aspects, diagnosis and treatment of trichinellosis. Expert Reviews in Anti-infection erapy, 1: 471– 482. Pozio, E., Hoberg, E., La Rosa, G. & Zarlenga, D.S. 2009. Molecular taxonomy, phylogeny and biogeography of nematodes belonging to the Trichinella genus. Infection Genetics and Evolution, 9(4): 606–616. Pozio, E. & Murrell, K.D. 2006. Systematics and epidemiology of Trichinella. Advances in Parasitology, 63: 367–439.

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A7.22 TRICHINELLA SPIRALIS General information Trichinella spiralis is an intracellular parasitic nematode of mammalian striated muscles. It is responsible for trichinellosis, a zoonosis resulting from consumption of raw or undercooked meat from infected animals (e.g. pork, game animals). Human outbreaks have been regularly reported during the last century (Ancelle et al., 2005; Khumjui et al., 2008). Trichinellosis is regarded as an emerging or reemerging disease in some parts of the world (particularly in Eastern Europe, Asia, etc.). Trichinella infections are mainly due to food or culinary habits, with pork being the major source of contamination for humans (Devine, 2003; Blaga et al., 2009). e Trichinella genus is divided in two clades (Gottstein, Pozio and Noeckler, 2009) with (i) encapsulated species due to the production of a collagen capsule surrounding the parasite: T. spiralis, T. nativa, T. britovi, T. murrelli, T. nelsoni, T. patagoniensis (Krivokapich et al., 2012) and 3 genotypes; and (ii) the non-encapsulated species that do not form a thick collagen capsule in muscle: T. pseudospiralis, T. papuae and T. zimbabwensis. Most of these species and genotypes are involved in human infections and clinical signs.

Geographical distribution It was estimated that more than 11 million people are infected worldwide (Dupouy-Camet, 2000), but this gure should be carefully used as it is based on serological studies. Even if Trichinella can be found worldwide in wild animals, the parasite is endemic in pig breeding in several countries in eastern Europe, Russia (in some areas), China (in various provinces), South Asia (Laos, ailand) and in South America (except Brazil). For example, an overall study in China described more than 500 human outbreaks, numbering 25 161 reported cases with 240 deaths (Liu and Boireau, 2002). It was underlined that this reported quantity was probably signi cantly underestimated because adequate diagnostic techniques might not have been available in China at the time.

Disease Severity of acute morbidity In animals the disease is considered as asymptomatic, whereas in humans, trichinellosis is a serious disease that can cause much su ering and rarely may result in death. e symptoms follow the parasitic life cycle, with an enteric phase, a migratory phase and a muscle phase. During the invasion of intestinal epithelium by the worms, intestinal pains and diarrhoea can be observed (Gottstein, Pozio and Noeckler, 2009). Severe signs and symptoms such as fever (39–40°C) and facial oedema may result from the migration of the larvae within blood vessels.

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e establishment of new-born larvae within the muscle cell and the encystment of muscle larvae (ML) are responsible for myalgia and asthenia. e most frequently a ected muscles are the muscles of the cervix, trunk, upper and lower extremities, and also less frequently the masseters. Severe myalgia generally lasts for two to three weeks. Severity of chronic morbidity and chronic illness fraction A small percentage of trichinellosis cases become “clinically chronic” and may be associated with recurrent muscle pain, a di culty in eye accommodation, and intestinal disorders in the case of repeated infection. Brain abnormalities were also reported by several authors (Gottstein, Pozio and Noeckler, 2009). e fraction of chronic illness is di cult to establish precisely as it depends on the initial infective dose of ML ingested and the density of ML spread in the organism. During large outbreaks, like those reported following the consumption of contaminated horse meat, less than 10% of human cases become chronic. Case fatality rates A study on the reported trichinellosis cases in China (Liu and Boireau, 2002) allowed for an estimate of mortality (0.9%). is gure con rmed the previous estimation for human mortality. Increase in human illness potential A recent report in India underlines the possibility of reaching 30% mortality in the absence of treatment during severe infection (Sethi et al., 2012).

Trade relevance Domestic pigs, horses and susceptible wild animals intended for human consumption are submitted to compulsory veterinary controls to ensure the meat is Trichinella free. e method for Trichinella detection is based on direct identi cation of the parasite a er arti cial digestion of muscle sample harvested on carcasses (Gajadhar et al., 2009). e reference method is described in both EU regulation and ICT (EU, 2005; ICT, no date) recommendations. Brie y, EU regulation requests that pigs must be systematically sampled at slaughterhouses and submitted to Trichinella detection (1 g for domestic swine, 2 g for breeding sows and boars, taken in the pillar of the diaphragm). Other animals (horse meat, wild game meat and other species sensitive to Trichinella infection) must be analysed with at least 5 g of muscle from tongue or jaw muscle for horsemeat and at least 5 g of muscle from foreleg, tongue or diaphragm for wild boar. Derogations for meat of domestic swine are possible when pig holdings have been o cially recognized as being controlled housing as de ned by the competent authorities.

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Impact on economically vulnerable populations Few studies on trichinellosis have been performed in low- or middle-income countries and there is a need for research in this eld.

Other relevant information Critical control points in pre- and post-harvest raising of pigs are described in OIE and ICT guidelines and also derogations are given in the EU regulation. e main points are: • Prevention of livestock contamination Feed must be purchased from an approved company that produces feed following good production practices. Feed and feed storage must be maintained in closed silos where rodents cannot enter. Feeding livestock with uncooked food waste, rodents or other wildlife are practices that expose animals to a risk of contamination by Trichinella. • Meat processing Meat of domestic swine that has undergone a freezing treatment according to EU regulation or ICT recommendations and under the supervision of competent authorities can be exempted from Trichinella examination. For example, pork of a thickness up to 15 cm needs to be frozen at -15°C for at least 20 days to be considered safe. However, Trichinella found in game meats (mainly T. nativa and to a lesser extent T. britovi) may be resistant to freezing and therefore frozen meat may still pose a public health risk. If meat cannot be controlled by a fully implemented direct examination, ICT recommends adequate treatment by cooking the meat to an internal temperature of 71°C. Appropriate treatment of meat cannot be ensured by the use of microwaves, drying or smoking. Prevention of human infection is accomplished by meat inspection, by meat processing and by prevention of exposure of food animals to infected meat. Game meats should always be considered as a potential source of infection, and therefore game meats should be tested or cooked thoroughly.

References Ancelle, T., De Bruyne, A., Poisson, D. & Dupouy-Camet, J. 2005. Outbreak of trichinellosis due to consumption of bear meat from Canada. France, September 2005. Eurosurveillance, 10(10: e051013.3) Blaga, R., Durand, B., Antoniu, S., Gherman, C., Cretu, C., Cozma, V. & Boireau, P. 2007. A dramatic increase in the incidence of human trichinellosis in Romania over the past 25 years: impact of political changes and regional food habits. American Journal of Tropical Medicine and Hygiene, 76: 983–986

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Devine, R. 2003. La consommation des produits carnés. INRA Productions Animales, 16: 325–327. Dupouy-Camet, J. 2000. Trichinellosis: a worldwide zoonosis. Veterinary Parasitology, 93: 191–200. EU (European Union). 2005. Commission Regulation (EC) No 2075/2005 of 5 December 2005 laying down speci c rules on o cial controls for Trichinella in meat. Available at http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2005:3 38:0060:0082:EN:PDF Accessed 2013-06-23. Gajadhar, A.A., Pozio, E., Gamble, H.R., Nockler, K., Maddox-Hyttel, C., Forbes, L.B., Vallee, I., Rossi, P., Marinculic, A. & Boireau, P. 2009. Trichinella diagnostics and control: mandatory and best practices for ensuring food safety. Veterinary Parasitology, 159: 197–205. Gottstein, B., Pozio, E. & Noeckler, K. 2009. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clinical Microbiology Reviews, 22: 127–145. ICT (International Commission on Trichinellosis). No date. Recommendations on methods for the control of Trichinella in domestic and wild animals intended for human consumption. Prepared by the ICT Standards for Control Guidelines Committee. 22 p. Available at http://www.trichinellosis.org/uploads/ICT_Recommendations_for_Control_English.pdf Accessed 2013-06-23. Khumjui, C., Choomkasien, P., Dekumyoy, P., Kusolsuk, T., Kongkaew, W., Chalamaat, M. & Jones, J.L. 2008. Outbreak of trichinellosis caused by Trichinella papuae, ailand, 2006. Emerging Infectious Diseases, 14: 1913–1915. Krivokapich, S.J., Pozio, E., Gatti, G.M., Gonzalez Prous, C.L., Ribicich, M., Marucci, G., La Rosa, G. & Confalonieri, V. 2012. Trichinella patagoniensis n.sp. (Nematoda), a new encapsulated species infecting carnivorous mammals in South America. International Journal for Parasitology, 42: 903–910 Liu, M. & Boireau, P. 2002. Trichinellosis in China: epidemiology and control. Trends in Parasitology, 18: 553–556. Sethi, B., Butola, K.S., Kumar, Y. & Mishra, J.P. [2012]. Multiple outbreaks of trichinellosis with high mortality rate. Tropical Doctor, 42(4): 243–243.

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A7.23 TRICHURIS TRICHIURA General information Trichuris trichiura is a nematode commonly known as the whipworm due to its particular shape (it looks like a whip with wider “handles” at the posterior end). Females are approximately 35–50 mm long, males 30–45 mm. e female T. trichiura produces 2000–10 000 single-celled eggs per day. Eggs are deposited from human faeces to soil where, a er two to three weeks depending on the temperature and humidity (hot and humid climatic conditions are optimal for their development), they become embryonated and enter the “infective” stage. When these embryonated infective eggs are ingested by humans, they hatch in the small intestine, exploiting the intestinal micro ora as hatching stimulus, where they grow and moult. e young worms move to the caecum and penetrate the mucosa with the cephalic end, and there they complete their development to adult worms. e life cycle from time of ingestion of eggs to development of mature worms takes approximately three months. During this time, there may be limited signs of infection in stool samples due to lack of egg production and shedding. e female T. trichiura begin to lay eggs a er three months of maturity, and worms can live up to two to three years.

Geographical distribution T. trichiura, together with Ascaris lumbricoides, Ancylostoma duodenal and Necator americanus, is a soil-transmitted helminth. It is distributed worldwide, infecting an estimated 600 million people, especially in tropical and subtropical areas, with the greatest numbers occurring in Africa, southern India, China, Southeast Asia and the Americas. In 2010, the global population at risk was estimated at 5 023 million (Asian Group Report, this publication), with a Global Burden of Disease (GBD) estimated at 1.0–6.4 million DALYs (WHO, 2102a) in the world (236 000 DALYs in Africa) (African Group Report, this publication). Infection occurs through ingestion of eggs by eating raw, unwashed vegetables, by drinking contaminated water, or by not washing the hands a er handling contaminated soil (a common transmission route for children).

Disease Morbidity is related to the number of worms harboured (WHO, 2012b). Light infections (<100 worms) are frequently asymptomatic, while bloody diarrhoea and dysentery may occur in heavy infections, with rectal prolapse possible in severe cases. Vitamin A de ciency may also result due to infection. Mechanical damage to the mucosa may occur, as well as toxic or in ammatory damage to the intestines of the host. Trichuriasis is one of the seven most common Neglected Tropical Diseases (NTDs) (GNNTD, 2012).

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Intensity of infection is classi ed by WHO according to the number of eggs per gram (epg) of faeces, excreted by infected persons: from 1–999 epg the infection is considered light, from 1000–9999 epg moderate, and >10 000 epg the infection is heavy intensity (WHO, 2011). e burden of disease due to T. trichiura is mainly attributed to its chronic and insidious impact on the health and quality of life of those infected, rather than to the mortality it causes. Infections of heavy intensity impair physical growth and cognitive development and are a cause of micronutrient de ciencies, leading to poor school performance and absenteeism in children, reduced work productivity in adults and adverse pregnancy outcomes. In countries of high endemicity of the soil-transmitted helminth parasites, preventive chemotherapy (i.e. repeated administration of anthelmintic drugs to at-risk populations) is the main strategy to control morbidity. However, rapid re-infection of humans occurs a er successful de-worming, and therefore e ective preventive measures are required to achieve public health goals with optimal e ciency and sustainability. In 2001, the World Health Organization endorsed preventive chemotherapy as the global strategy to control soil-transmitted helminthiasis (WHO, 2012b). e key component of this strategy is regular administration of anthelmintic drugs to at-risk groups: children, women of childbearing age, and adults in high-risk occupations, such as nightsoil re-use and farming. Although this strategy reduces illness caused by soil-transmitted helminths, it does not prevent rapid re-infection. To interrupt transmission and to achieve local elimination of helminthiasis, integrated control approaches that include access to sanitation and other complementary interventions of a primary prevention nature are needed (Ziegelbauer, 2012).

Trade relevance Currently this parasite is not considered an issue in trade. Due to the faecal-oral route of transmission for T. trichiura, the primary production and pre-harvest stage of the food chain are critical in terms of control of this parasite, and areas for cultivation of fresh produce, particularly for raw consumption, need to be assessed in terms of their susceptibility to faecal contamination.

Impact on economically vulnerable populations Poor hygiene, especially lack of sanitation occurring wherever there is poverty, is associated with soil-transmitted helminthiases, such as T. trichiura, and also contributes to the faecal contamination of foods. People infected with soil-transmitted helminths have parasite eggs in their faeces. In areas where there are no latrine

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systems, the soil (and water) around the village or community becomes contaminated with faeces containing worm eggs. Children are especially vulnerable to infection due to their high exposure risk.

References GNNTD (Global Network on Neglected Tropical Diseases). 2012. Web site. http:// www.globalnetwork.org/trichuriasis Accessed 2013-06-23. WHO (World Health Organization). 2011. Helminth control in school age children. A guide for managers of control programmes. 2nd ed. 90 p. Available at http:// whqlibdoc.who.int/publications/2011/9789241548267_eng.pdf Accessed 201306-23. WHO. 2012a. Research priorities for helminth infections. Technical report of the TDR disease reference group on helminth infections. WHO Technical Report Series, no. 972. 174 p. Available at http://apps.who.int/iris/bitstream/10665/75922/1/WHO_ TRS_972_eng.pdf Accessed 2013-06-23. WHO. 2012b. Soil-transmitted helminthiases: eliminating soil-transmitted helminthiases as a public health problem in children. Progress report 2001–2010 and strategic plan 2011–2020. 79 p. Available at http://whqlibdoc.who.int/publications/2012/9789241503129_eng.pdf Accessed 2013-06-23. Ziegelbauer, K., Speich, B., Mäusezahl, D., Bos, R., Keiser, J. & Utzinger, J. 2012. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Medicine, 9(1): e1001162. Online; doi: 10.1371/journal. pmed.1001162.

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A7.24 TRYPANOSOMA CRUZI General information Chagas disease, or American trypanosomiasis, a primarily vector-borne parasitic disease in the Americas, is a human infection caused by the protozoan parasite Trypanosoma cruzi. e disease can also be transmitted through transfusion, through transplant, congenitally and by oral transmission (WHO, 2003; Bern et al., 2011). T. cruzi is a agellate that belongs to the Kinetoplastida order, Trypanosomatidae family, characterized by the presence of one agellum and a single mitochondrion, where the kinetoplast is located. e parasite T. cruzi is not a homogeneous population and is composed of a pool of strains which circulate both in the domestic and sylvatic cycles involving humans, vectors and animal reservoirs of the parasite (Bern et al., 2011).

Geographical distribution According to information from 21 countries located throughout Mexico, Central America and South America, where the disease is endemic, the number of infected people today is estimated at 7 694 500 (1.448% of the population) (PAHO/WHO, 2012). e number of new cases per year due to vector transmission is estimated at 41 200 (7775 per 100 000) and the number of new cases of congenital Chagas disease per year has been estimated at 14 385. In addition, in 2008, 11 000 people died from the disease (WHO, 207; PAHO/WHO, 2012; WHO. 2010). Animal reservoirs To date, over 100 mammalian species have been reported as natural hosts for T. cruzi, and all mammals are considered to be susceptible to infection. e epidemiologically important reservoirs vary geographically according to the biology and ecology of mammals and vectors, and how these interactions translate to risk of human exposure. Although T. cruzi has a wide host range, opossums and armadillos are important reservoirs throughout the Americas (Bern et al., 2011). Vectors ere are more than 130 triatomine species (blood sucking reduviid insects) in the Americas, many of which can be infected by and transmit T. cruzi. However, a small number of highly domiciliated vectors are important in the human epidemiology of the disease. e major triatomine species that colonize domestic and peridomestic environments and play an important role in the epidemiology of Chagas disease in Latin America are: Triatoma infestans in Argentina, Brazil, Chile, Paraguay, southern Peru and Uruguay; Rhodnius prolixus in Colombia, El Salvador, Guatemala, Honduras, southern Mexico, Nicaragua and Venezuela; Triatoma dimidiate in Belize, Colombia, Costa Rica, Ecuador, El Salvador, Guatemala, Honduras, Mexico, Nicaragua, Panama, northern Peru and Venezuela;

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Panstrongylus megistus in Argentina, Brazil, Paraguay, Uruguay; and Triatoma brasiliensis in north-eastern Brazil (WHO, 2003; Bern et al., 2011).

Disease In the Americas, T. cruzi infection is most commonly acquired through contact with faeces of an infected triatomine bug (vector-borne transmission) that can enter the human body through a bite wound, intact conjunctiva or other mucous membranes. Infection can also occur from: mother-to-baby (congenital), contaminated blood products (transfusions), transplanted organs from infected donors, laboratory accidents, food or drink contaminated with vector faeces (oral transmission) or consumption of raw meat from infected mammalian sylvatic hosts (Nóbrega et al., 2009; Dias, Amato Neto and Luna, 2011; Toso, Vial and Galanti, 2011; PAHO, 2009). e acute phase of infection usually lasts around two months immediately a er infection and is characterized by a variety of clinical manifestations and parasites that may be found in the blood. Most cases have no or few symptoms, but there may be a skin chancre (chagoma) or unilateral purplish orbital oedema (Romaña’s sign) with local lymphadenopathy and fever over several weeks. More general symptoms include: headache, myalgia, dyspnoea, oedema in inferior extremities or face, abdominal pain, cough, hepatomegaly, rash, painful nodules, splenomegaly, generalized oedema, diarrhoea, multiple lymphadenopathy, myocarditis and, more rarely, meningoencephalitis Following the acute phase, most infected people enter into a prolonged asymptomatic form of the disease (called ‘chronic indeterminate’) during which few or no parasites are found in blood, but with positive anti-T. cruzi serology. However, 10–40% will go on over the next decades to develop cardiac or digestive manifestations, or both. Cardiac sequelae include: conduction disorders, arrhythmia, cardiomyopathy, heart failure, cardiac aneurysm and secondary thromboembolism. Digestive lesions include megaoesophagus and megacolon (WHO, 2003; Bern et al., 2011).

Chagas disease by oral transmission Following advances in the control of vectors and transmission of Chagas disease via blood transfusion in the endemic regions of America, alternative mechanisms of transmission have become more important, and several outbreaks reported in Brazil, Colombia and Venezuela have occurred due to transmission of T. cruzi through an oral route and have been attributed to contaminated fruit, palm wine or sugar cane juice (Nóbrega et al., 2009; Alarcón de Noya et al., 2010; Dias, Amato Neto and Luna, 2011; Toso, Vial and Galanti, 2011; PAHO, 2009).

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e clinical presentation of Chagas disease contracted through oral transmission is di erent from that observed in vector-borne infection, with more severe acute morbidity and higher mortality. A er an incubation period of 5 to 22 days postingestion, the disease is expressed with acute manifestations of fever, gastric irritation, abdominal pain, vomiting, jaundice and bloody diarrhoea. As a result, in many cases patients develop severe myocarditis and meningeal irritation. Lethality can reach a relatively high level (up to 35.2%, with an average rate of 7.1%) (Alarcón de Noya et al., 2010; PAHO, 2009; Bern et al., 2011).

Trade relevance e food-borne transmission route for T. cruzi is a new, emerging hazard, and the extent of the possible trade impact has not been fully assessed. e precise stage of food handling at which contamination occurs is unknown, although various foods, such as fruit juice, sugar cane and açaí palm, are involved, possibly contaminated with infected triatomine faeces during processing. Oral transmission of Chagas disease is always dependent on infected vectors or reservoirs as T. cruzi does not multiply in food, therefore the disease is relevant in countries with vector-borne transmission and, additionally, outbreaks contracted through oral transmission have been detected. e adoption of good food hygiene measures, as well as proper cooking of wild meat from endemic areas minimizes the risk of transmission. In the case of prepared foods produced in areas with triatomine bugs, high standards of proper cooking or pasteurization become essential. Pasteurization of açaí pulp is being adopted for the product exported to other regions of the Amazon in Brazil and abroad (Dias, Amato Neto and Luna, 2011; PAHO, 2009).

Impact on economically vulnerable populations Food-borne transmission of T. cruzi may occur more o en than is currently recognized. Most outbreaks are small, o en a ecting family groups in rural areas, and unusually in urban populations of South America (Nóbrega et al., 2009; Alarcón de Noya et al., 2010; Dias, Amato Neto and Luna, 2011; Toso, Vial and Galanti, 2011). is form of transmission is considered an emerging threat to public health; the negative socio-economic impact is due to the high morbidity and mortality in the community a ected by outbreaks.

References Alarcón de Noya, B., Díaz-Bello, Z., Colmenares, C., Ruiz-Guevara, R., Mauriello, L., Zavala-Jaspe, R., Suarez, J.A., Abate, T., Naranjo, L., Paiva, M., Rivas, L., Castro, J., Márques, J., Mendoza, I., Acquatella, H., Torres, J. & Noya, O. 2010. Large

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urban outbreak of orally acquired acute Chagas disease at a school in Caracas, Venezuela. Journal of Infectious Diseases, 201(9): 1308–1315. Bern, C., Kjos, S., Yabsley, M.J. & Montgomery, S.P. 2011. Trypanosoma cruzi and Chagas’ Disease in the United States. Clinical Microbiology Reviews, 24(4): 655–681. Dias, J.C., Amato Neto V. & Luna, E.J. 2011. [Alternative transmission mechanisms of Trypanosoma cruzi in Brazil and proposals for their prevention] [Article in Portuguese]. Revista da Sociedad Brasileira de Medicina Tropical, 44(3): 375–379. Nóbrega, A.A., Garcia, M.H., Tatto, E., Obara, M.T., Costa, E., Sobel, J. & Araujo, W.N. 2009. Oral transmission of Chagas disease by consumption of açaí palm fruit, Brazil. Emerging Infectious Diseases, 15(4): 653–655. PAHO (Pan-American Health Organization). 2009. Guía para vigilancia, prevención, control y manejo clínico de la enfermedad de Chagas aguda transmitida por alimentos. [In Spanish] – Rio de Janeiro: PANAFTOSA-VP/OPAS/OMS, 2009. 92 p. (Serie de Manuales Técnicos, 12). Doc. PAHO/HSD/CD/539.09. Available at http://bvs.panalimentos.org/local/File/Guia_Enfermedad_Chagas_2009esp.pdf Accessed 2013-06-23. PAHO/WHO. 2012. Fact sheet. [Estimación cuantitativa de la enfermedad de Chagas en las Américas] [In Spanish]. Doc. OPS/HDM/CD/425.06. Available at http://new. paho.org/hq/index.php?option=com_content&view=article&id=5856&Itemid=41 96&lang=es Accessed 2013-06-23. Toso M., A., Vial F., U. & Galanti, N. 2011. Oral transmission of Chagas’ disease. Revista Medica de Chile, 139(2): 258–266. WHO (World Health Organization). 2003. Control of Chagas disease: second report of the WHO Expert Committee. Prepared by WHO Expert Committee on the Control of Chagas Disease. OMS Serie de informes técnicos, no. 905. 117 p. Available at http://apps.who.int/iris/bitstream/10665/42738/1/WHO_TRS_905_spa.pdf Accessed 2013-06-23. WHO. 2007. Reporte del Grupo de trabajo cientí co sobre la enfermedad de Chagas, Buenos Aires, Argentina, 17–20 April 2005. Edited by F. Guhl and G. Lasdinz. WHO Doc. TDR/GTC/09. Available at http://whqlibdoc.who.int/hq/2007/TDR_ SWG_09_spa.pdf Accessed 2013-06-23. WHO. 2010. Enfermedad de Chagas: control y eliminación: Informe de la Secretaría A63/17 22 de abril de 2010. Paper prepared for the 63rd World Health Assembly. Geneva, Switzerland. 5 p. Available at http://apps.who.int/iris/bitstream/10665/4877/1/A63_17-sp.pdf Accessed 2013-06-23.

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A7.25 GLOSSARY OF PARASITOLOGICAL TERMS assemblage – the preferred term for a Giardia duodenalis genotype bradyzoite – the slowly multiplying life cycle stage of some coccidian parasites (e.g. Toxoplasma gondii); found inside tissue cysts in host cells cestode – tapeworm (Phylum Platyhelminthes, Class Cestoda); all are parasitic (e.g. Diphyllobothrium spp., Echinococcus spp., Taenia spp.) coccidian – member of a group of protozoan parasites (Phylum Apicomplexa) that inhabit cells lining the host’s intestinal tract (e.g. Cryptosporidium spp., Cyclospora cayetanensis, Toxoplasma gondii) cyst – environmental life cycle stage of some protozoan parasites, containing trophozoites (e.g. Entamoeba histolytica, Giardia duodenalis,); may also refer to tissue cysts of Toxoplasma gondii, sarcocysts of Sarcocystis spp., or hydatid cysts of Echinococcus spp. cysticercus (pl. cysticerci) – the infectious larval stage of some tapeworms (e.g. Taenia spp.) DALY (or DALYs) – Disability-Adjusted Life Year; a measure of disease burden calculated by adding YLL and YLD de nitive host – the nal host in the life cycle of a parasite and in which sexual reproduction occurs, resulting in the production of the infectious environmental stage (e.g. eggs, cysts or oocysts) encyst (encystment or encystation) – the formation of an environmentally-resistant cyst around some protozoan parasites prior to their shedding with the host’s faeces (e.g. Giardia duodenalis); a result of physiological and biochemical triggers within the host’s digestive tract; also, the formation of a cyst around helminth larvae at the beginning of the dormant tissue phase of the life cycle (e.g. Taenia spp., Trichinella spp.) excyst (excystment or excystation) – release of motile, infective life cycle stages of protozoan parasites following ingestion of cysts or oocysts by a host genotype – a genetically distinct group of organisms within a species genus – a taxonomic group of organisms with similar attributes consisting of one or more species; typically written in italics followed by the species name

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helminth – worms belonging to four phyla: Nematoda (roundworms), Platyhelminths ( atworms e.g. cestodes and trematodes), Acanthocephala (spiny-headed worms) and Nemathophora (hairworms) hexocanth – see: oncosphere hydatid cyst – uid- lled cyst containing larvae (protoscoleces) of the tapeworm, Echinococcus spp.; they develop in liver, lungs, brain and other organs of the intermediate host incubation period – the period of time between exposure to a parasite and the rst symptoms intermediate host – a host in the life cycle of a parasite in which some speci c developmental stage is reached, short of the sexually mature stage; the parasite is subsequently transmitted to the next intermediate host, or to the de nitive host, through predation, accidental ingestion or freeliving larvae Loe er’s syndrome – a disease in which eosinophils accumulate in the lung in response to a parasitic infection (e.g. Ascaris lumbricoides ) metacercariae (sing. metacercaria) – encysted infectious larval stage of trematodes; found in the tissues of intermediate hosts (e.g. Clonorchis sinensis) or attached to aquatic vegetation (e.g. Fasciola hepatica) merozoite – non-motile life cycle stage of coccidian parasites; produced during the asexual cycle in cells lining the host’s intestinal tract metacestode – the larval stage of a tapeworm found in an intermediate host (e.g. cysticercus, hydatid cyst) nematode – roundworm (Phylum Nematoda); includes parasitic species (e.g. Anisakidae, Ascaris spp., Toxocara spp., Trichinella spp.) OLM – ocular larval migrans oncosphere – the embryo of some tapeworms (e.g. Echinococcus spp., Taenia spp.) which has six hooklets and is surrounded by a membrane and contained within an egg; also referred to as a hexacanth oocyst – the infectious environmental stage of coccidian parasites, produced through the sexual stage of the life cycle

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paratenic host – a host not necessary for the development of a parasite but which may facilitate the completion of its life cycle and its dispersion in the environment. In contrast to its development in a secondary host, a parasite in a paratenic host does not undergo any changes into the following stages of its development. plerocercoid – a larval stage of some cestodes with aquatic life cycles (e.g. Diphyllobothrium spp.); found in tissues of the second intermediate host procercoid – a larval stage of some cestodes with aquatic life cycles (e.g. Diphyllobothrium spp.); found in the rst intermediate host proglottids – the “segments” of tapeworms; mature proglottids contain both male and female reproductive organs, while gravid proglottids consist of uteri lled with eggs protoscolex (pl. protoscoleces) – juvenile scolex of some tapeworms (e.g. Echinococcus spp.,Taenia spp.) which bud from the inner lining of the cyst protozoan – single-celled eukaryotic organism; this group includes parasitic species (e.g. Cryptosporidium spp., Cyclospora cayetanensis, Giardia duodenalis, Toxoplasma gondii) redia – a digenean trematode ( uke) in the larval stage developed from a sporocyst in the main intermediate host, and in turn forming a number of cercariae scolex (pl. scoleces) – the “head” or anterior end of tapeworms; equipped with hold-fast structures such as suckers, grooves or hooks, or a combination species (sing. sp., pl. spp.) – a taxonomic group of organisms within a genus which is distinct from other species based on morphological, biological, and molecular characteristics; the genus and species make up the “scienti c name” (Latin binomial) of an organism, and are typically written in italics sporocyst – structures containing sporozoites found within mature oocysts of some coccidian parasites; also, a cyst which contains the rediae larvae of some trematode parasites sporozoite – motile, infective life cycle stage of coccidian parasites; released from mature oocysts upon ingestion by a host; may be contained within sporocysts

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sylvatic – referring to diseases a ecting and/or cycling through wild animals; distinguished from domestic or synanthropic cycles synanthropic – referring to diseases or pathogens whose life cycles are ecologically associated with humans and domestic animals; distinguished from sylvatic cycles tachyzoite – motile life cycle stage of some coccidian parasites (e.g. Toxoplasma gondii); undergo rapid multiplication in the host before developing into bradyzoites and forming tissue cysts tissue cyst – cluster of Toxoplasma gondii bradyzoites surrounded by a cyst wall within cells of the host’s organs and tissues trematode – uke (Phylum Platyhelminthes, Class Trematoda); all are parasitic (e.g. Fasciola spp., Heterophyidae, Opisthorchiidae, Paragonimus spp.) trophozoite – the motile, asexually multiplying stage in the life cycle of many protozoan parasites; present in host cells or attached to cells lining the intestine viscera – the internal organs of the body; particularly in the thoracic and abdominal cavities VLM – visceral larval migrans YLL – a metric describing the Years of Life Lost in a population due to di erent factors, including infectious diseases YLD – a metric describing the Years Lost due to Disability in a population due to various factors, including infectious diseases zoonosis (noun.) – a disease naturally transmitted from one species of animal to another (including those transmitted through a vector), especially to humans zoonotic (adj.) – designating, causing or involving a zoonosis; transmitted from animals to humans

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Annex 8 Regional Reports e experts were grouped into seven geographical regions and were asked to prepare and bring to the meeting regional information that considered the current overall quantity and quality of data at the regional and global levels; burden of disease and food attribution; data on parasite prevalence; incidence and concentration in the main food categories; agri-food trade; consumer perception; social sensitivity; and risk management options. ese reports were used by the experts in their deliberations during the meeting. e seven geographical regions represented were Africa, Asia, Paci c (primarily Australia), Europe, Near East, North America and South America. What little that was available for Central America was added to the North America section. Note on information sources: e references for the Asia regional report were revised a er the meeting, and a few were updated (2013). Note on taxonomy: ere has been confusion concerning the causative agent of giardiasis, and it has variously been named as Giardia duodenalis, Giardia lamblia or Giardia intestinalis. e general consensus is that the parasite should be identied as Giardia duodenalis, with Giardia lamblia and Giardia intestinalis considered synonyms.

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ANNEX 8.1 AFRICA A8.1.1 Introduction e group members (Erastus Kang’ethe, Kenya; Allal Dakkak, Morocco; and Samson Mukaratirwa, South Africa) were responsible for collating data on foodborne parasites relevant to the African region, deriving the information from the proposed list and based on their experiences and information available in the literature. Communication and exchange of information among members of the group was through e-mail. Samson Mukaratirwa, as the Group leader, was responsible for compiling the contributions from members, following the speci c guidelines from the Secretariat of the FAO/WHO Joint Expert Meetings on Risk Assessment (JEMRA).

A8.1.2 Data availability in humans, and food attribution To some extent data is available on the prevalence of Taenia solium, T. saginata, Echinococcus granulosus and Toxoplasma gondii, but not enough to quantify the burden of the disease in humans in the region. In many African countries there is virtually no data on prevalence in humans, and there is a general lack of surveillance systems, which leads to no availability of data to quantify the burden of the disease. With the advent of the HIV-AIDS pandemic in sub-Saharan Africa there are reports of cases of cryptosporidiosis and toxoplasmosis, but mainly in immuno-compromised individuals. E orts have been made in the last decade to estimate the burden of T. solium cysticercosis in sub-Saharan Africa, with some success in Cameroon and South Africa, and in Africa as whole the burden of ascariasis and trichuriasis has been estimated. For other foodborne parasites, more prevalence studies are needed to quantify the disease burden. in humans Although parasites like Toxoplasma gondii, Giardia spp., Cryptosporidium spp. and Trichinella spp. have a global importance, they are still very much underreported in Africa, either because of lack of prioritization by relevant authorities or by being overshadowed by the importance of other parasites, such as Plasmodium spp. ere is need to collect data on the prevalence of these parasites in order to estimate the burden of the disease in the region, especially for neglected rural communities, where the prevalence is assumed to be very high.

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TABLE A8.1.1 Data availability on the burden of disease and food attribution at the regional and global level for Africa Regional level Disease severity/ main populations at risk Yes [28, 30, 33] High prevalence in sub-Saharan Africa Main mode of transmission is via skin penetration. Oral transmission through ingestion of contaminated vegetables and drinking water may occur. Children are at high risk [28, 32, 33] Contaminated water, fruits and edible plants [27] Yes [27] Yes [27] 1 851 000 DALYs in the world. Yes [22, 23] Yes [22] Yes [28, 32] Yes [28, 32] [28, 32] Main food source and attribution Disease in humans Disease severity/ main populations at risk Main food sources and attributions Global level

Data availability on human disease related parameters

Parasite species

Disease in humans

Ancylostoma duodenale

Yes [28, 33] North Africa: 0–1.9%; Central Africa: 10–20%; South and West Africa: 50-70%.

Ascaris lumbricoides

Yes [27]

Yes [27] 91333.5 000 DALYs in Africa

Contaminated water, fruits and edible plants [27] Mainly contaminated water and edible plants [22]

Cryptosporidium spp.

Yes [21] Mainly in immunocompromised individuals.

Yes Related to urban dwellers with poor supply of potable water and HIV-infected. High pathogenic e ects in children aged 6 to 36 months, particularly those who are malnourished or positive for HIV infection. Yes [14, 15] Young children are most o en a ected because of their constant hand-to-mouth behaviour

Mainly contaminated water, fruits and edible plants

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Echinococcus granulosus

Yes [12, 13, 14, 15] Hydatidosis is highly prevalent and 3 to 7 surgical cases per 100 000 inhabitants a year in sub-Saharan Africa. There is rather conspicuous concentration of human cases in NW Sudan, NE Uganda, SE Ethiopia and extreme SE Sudan.

Edible fruits, plants and water contaminated with eggs [14, 15]

Yes [16] Cystic hydatidosis is one of the most important zoonotic diseases

Yes [17] Global DALYs lost due to disease is estimated at 285 407

Edible plants, fruits and water contaminated with eggs

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174 Regional level Disease severity/ main populations at risk Yes [10. 11] Scanty reports for the disease in humans. Main populations at risk are rural communities with poor sanitation. Disease is not considered as severe in humans. Meat [10. 11] (undercooked or raw beef) Yes [11] Main food source and attribution Disease in humans Disease severity/ main populations at risk Global level Main food sources and attributions Yes [11] Meat [11] Population undercooked in areas or raw beef where poor sanitation and animal husbandry facilitate parasite transmission Yes [7, 8] Yes [7] Meat (undercooked or raw pork); edible raw plants and fruits contaminated with eggs; autoinfection [8]

Data availability on human disease related parameters

Parasite species

Disease in humans

Taenia saginata

Yes [9, 10] Not many studies conducted in humans and in many instances there is di culty in di erential Dx with T. solium eggs. Occurs in most African countries, but the epidemiological patterns in the African countries are far from being complete. Yes [3. 4, 5, 6] Underestimated because of lack of cheap and reliable Dx test. Monetary burden valued at US$ 34.2 million in the Eastern Cape Province of South Africa. 9.0 DALYs lost per 1000 persons in Cameroon. Meat (undercooked or raw pork); edible raw plants and fruits contaminated with eggs; autoinfection

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Taenia solium

Yes [1. 2] Except for the Muslim regions, where pork is not eaten for religious reasons, T. solium cysticercosis a ects virtually all countries in Western and Central Africa West Africa: 0.6–17%; Central Africa: 0.6–20%; West Africa: 0.1–6.5%. Neurocysticercosis is considered to be the commonest parasitic disease of the human nervous system

Data availability on human disease related parameters Regional level Disease severity/ main populations at risk Yes [19] Reports related to HIV infection and congenital infections. Yes Milk and raw or undercooked meat from livestock contaminated with tachyzoites and bradyzoites; drinking of water and ingestion of edible plants contaminated with oocysts. Yes [8] High seroprevalence in North America (10%) and UK (40%); 50 to 80% in continental Europe and Latin America. However, prevalence is steadily decreasing. Yes [27] Yes [27] 1 012 000 DALYs in the world Yes [26] Yes [26] About 11 million people may be infected Yes Due to HIV-AIDS pandemic in sub-Saharan Africa. Main food source and attribution Disease in humans Disease severity/ main populations at risk Main food sources and attributions Milk and raw or undercooked meat from livestock contaminated with tachyzoites and bradyzoites; drinking of water and ingestion of edible plants contaminated with oocysts [8] Contaminated water, fruits and edible plants [27] Meat [26] undercooked or raw meat and products from pigs, horses and wildlife of temperate regions, like bears and seals. Global level

Parasite species

Disease in humans

Toxoplasma gondii Yes [18] Mainly in immunocompromised individuals. Occurs in most African countries, where it seems to be frequent, but the epidemiological patterns in the African countries are far from clear. The prevalence of infection seems to be high and varies from 15 to 60%.

Trichuris trichiura

Yes [27]

Yes [27] 236 000 DALYs in Africa

Contaminated water, fruits and edible plants [27]

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Trichinella spp

Yes [24] Sporadic cases reported in Africa. Species identi cation from cases not always done.

Yes Sporadic clinical cases con rmed in humans but species not determined.

Meat (undercooked or raw meat and products from wild pig, warthog, bush pig).

Notes: Dx = diagnostic; DALY = disability-adjusted life year

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Sources used for Table A8.1.1: 01. O’Neal, S.E., Townes, J.M., Wilkins, P.P., Noh, J.C., Lee, D., Rodriguez, S., Garcia, H.H. & Stau er, W.M. 2012. Seroprevalence of antibodies against Taenia solium cysticerci among refugees re-settled in United States. Emerging Infectious Diseases, 18(3): 431-438. Zoli, A., Shey-Njila, O., Assana, E., Nguekam, J.P. , Dorny, P., Brandt, J. & Geerts, S. 2003. Regional status, epidemiology and impact of Taenia solium cysticercosis in Western and Central Africa. Acta Tropica, 87(1) 35–42. Phiri, I.K., Ngowi, H., Afonso, S. and 16 others. 2003. The emergence of Taenia solium cysticercosis in Eastern and Southern Africa as a serious agricultural problem and public health risk. Acta Tropica, 87(1): 13–23. Carabin, H., Krecek, R.C., Cowan, L.D., Michael, L., Foyaca-Sibat, H., Nash, T. & Willingham, A.L. 2006. Estimation of the cost of Taenia solium cysticercosis in Eastern Cape Province, South Africa. Tropical Medicine & International Health, 11(6): 906–916. Praet, N., Speybroeck, N., Manzanedo, R., Berkvens, D., Nforninwe, D.N., Zoli, A., Quet, F., Preux, P.M., Carabin, H. & Geerts, S. 2009. The Disease Burden of Taenia solium Cysticercosis in Cameroon. PLOS Neglected Tropical Diseases, 3(3): Art. No. e406. Newell, E., Vyungimana, F., Geerts, S., VanKerckhoven, I., Tsang, V.C.W. & Engels, D. 1997. Prevalence of cysticercosis in epileptics and members of their families in Burundi. Transactions of the Royal Society of Tropical Medicine and Hygiene, 91(4): 389–391. Pawlowski, Z., Allan, J. & Sarti, E. 2005. Control of Taenia solium taeniasis/cysticercosis: From research towards implementation. International Journal for Parasitology, 35(1112): 1221–1232. Gajadhar, A.A., Scandrett, W.B. & Forbes, L.B. 2006. Overview of food- and water-borne zoonotic parasites at the farm level. Revue Scienti que et Technique de l’OIE, 25(2): 595– 606. Biu, A.A. & Hena, S.A. 2008. Prevalence of human Taeniasis in Maiduguri, Nigeria. International Journal of Biomedical and Health Sciences, 4(1): 25–27; Karrar, Z.A. & Rahim, F.A. 1995. Prevalence and risk-factors of parasitic infections among under-5 Sudanese children – a community-based study. East African Medical Journal, 72(2): 103– 109. Benazzou, S., Arkha, Y., Derraz, S., El Ouahabi, A. & El Khamlichi, A. 2010. Orbital hydatid cyst: Review of 10 cases. Journal of Cranio-Maxillofacial Surgery, 38(4): 274–278. Knight-Jones, T.J.D., Mylrea, G.E. & Kahn, S. 2010. Animal production food safety: priority pathogens for standard setting by the World Organisation for Animal Health. Revue Scienti que et Technique OIE, 29(3): 523–535. Magambo, J., Njoroge, E. & Zeyhle, E. 2006. Epidemiology and control of echinococcosis in sub-Saharan Africa. Parasitology International, 55(Suppl.): S193–S195. Elmahdi, I.E., Ali, Q.M., Magzoub, M.M.A., Ibrahim, A.M., Saad, M.B. & Romig, T. 2004. Cystic echinococcosis of livestock and humans in central Sudan. Annals of Tropical Medicine and Parasitology, 98(5) 473–479; Mersie, A. 1993. Survey of echinococcosis in eastern Ethiopia. Veterinary Parasitology, 47(1-2): 161–163. Dakkak, A. 2010. Echinococcosis/hydatidosis: A severe threat in Mediterranean countries. Veterinary Parasitology, 174(1-2): 2–11. Romig, T., Omer, R.A., Zeyhle, E., Huttner, M., Dinkel, A., Siefert, L., Elmahdi, I.E., Magambo, J., Ocaido, M., Menezes, C.N., Ahmed, M.E., Mbae, C., Grobusch, M.P. & Kern, P. 2011. Echinococcosis in sub-Saharan Africa: Emerging complexity. Veterinary Parasitology, 181(1 – Special Issue): 43–47. Jenkins, D.J., Romig, T. & Thompson, R.C.A. 2005. Emergence/re-emergence of Echinococcus spp. – a global update. International Journal for Parasitology, 35(1112): 1205-1219; Matossian, R.M., Rickard, M.D. & Smyth, J.D. 1977. Hydatidosis: a global problem of increasing importance. Bulletin WHO, 55(4): 499–507

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03.

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17.

Battelli, G. 2009. Echinococcosis: costs, losses and social consequences of a neglected zoonosis. Veterinary Research Communications, 33: S47–S52; Budke, C.M., Deplazes, P. & Torgerson, P.R. 2006. Global socioeconomic impact of cystic echinococcosis. Emerging Infectious Diseases, 12(2): 296–303; Torgerson, P.R. 2010. Financial burdens and Disability-Adjusted Life Years in echinococcosis. pp. 1373–1389 (Pt 2, 2.5), in: V.R. Preedy and R.R. Watson (editors). Hand book of diseases burden and quality of life measures. Springer Reference. Dubey, J.P., Tiao, N., Gebreyes, W.A. & Jones, J.L. 2012. A review of toxoplasmosis in humans and animals in Ethiopia. Epidemiology and Infection , 140(11): 1935–1938; Bisvigou, U., Mickoto, B., Ngoubangoye, B., Mayi, T.S., Akue, J.P. & Nkoghe, D. 2009. Seroprevalence of toxoplasmosis in a rural population in south-eastern Gabon. Parasite – Journal de la Societe Francaise de Parasitologie, 16(3): 240–242; Joubert, J.J. & Evans, A.C. 1997. Current status of food-borne parasitic zoonoses in South Africa and Namibia. Southeast Asian Journal of Tropical Medicine and Public Health, 28(Suppl. 1): 7–101. Lucas, S.B., Hounnou, A., Peacock, C. and 15 others. 1993. The mortality and pathology of HIV infection in a West African city. AIDS, 7(12): 1569–1579. Bogaerts, J., Lepage, P., Rouvroy, D. & Vandepitte, J. 1984. Cryptosporidium spp., a frequent cause of diarrhea in central Africa. Journal of Clinical Microbiology, 20(5): 874–876; Peng, M.M., Meshnick, S.R., Cunli e, N.A., Thindwa, B.D.M., Hart, C.A., Broadhead, R.L. & Xiao, L.H. 2003. Molecular epidemiology of cryptosporidiosis in children in Malawi. Journal of Eukaryotic Microbiology, 50(Suppl.): 557–559; Samie, A., Bessong, P.O., Obi, C.L., Sevilleja, J.E.A.D., Stroup, S., Houpt, E. & Guerrant, R.L. 2006. Cryptosporidium species: Preliminary descriptions of the prevalence and genotype distribution among school children and hospital patients in the Venda region, Limpopo Province, South Africa. Experimental Parasitology, 114(4): 314–322. Savioli, L. & Thompson, A. 2006. Giardia and Cryptosporidium join the ‘Neglected Diseases Initiative’. Trends in Parasitology, 22(5): 203–208. Gaash, B. 2006. Cryptosporidiosis. Indian Journal for the Practising Doctor, 3(1): 2006-03 – 2006-04. [Online; see http:/ /www.indmedica.com/journals.php?journalid=3&issueid=7 4&articleid=955&action=article ] Dupouy-Camet, J., Lecam, S., Talabani, H. & Ancelle, T. 2009. Trichinellosis acquired in Senegal from warthog ham, March 2009. Eurosurveillance, 14(21): 63–64 [Art. No. 19220]; Pozio, E. 2007. World distribution of Trichinella spp. infections in animals and humans. Veterinary Parasitology, 149(1-2 Special Issue): 3–21.

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19. 21.

22. 23.

24.

26. 27.

Dupouy-Camet, J. 2000. Trichinellosis: a worldwide zoonosis. Veterinary Parasitology, 93(3-4): 191–200. WHO (World Health Organization). 2008. The global burden of disease: 2004 update. Available at: http:/ /www.who.int/healthinfo/global_burden_disease/2004_report_ update/en/ Haburchak, D.R. 2011. Ascariasis – Pathophysiology. [Online Medscape antry; dated 2011-11-21; accessed 2013-05-31] See: http:/ /emedicine.medscape.com/article/212510overview#a0104 Jiraanankul, V., Aphijirawat, W., Mungthin, M., Khositnithikul, R., Rangsin, R., Traub, R.J., Piyara,j P., Naaglor, T., Taamasri, P. & Leelayoova, S. 2011. Incidence and risk factors of hookworm infection in a rural community of central Thailand. American Journal of Tropical Medicine and Hygiene, 84(4): 594–598. Palmer, P.E.S. & Reeder, M.M. [2008]. The Imaging of Tropical Diseases. See Chapter 12. Online – see http:/ /tmcr.usuhs.mil/tmcr/sta .htm. Originally published by SpringerVerlag, Berlin, Germany.

28.

31.

33.

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TABLE A8.1.2 Data availability for parasite prevalence or concentration in the main food categories for Africa Taenia saginata Beef Game Yes {6–9] Yes {6–9]

Echinococcus granulosus Beef Game Other Taenia solium Pork Fruits Vegetables Other Yes [1–5] Yes [1–5] Contaminated with T. solium eggs. Yes [1–5] Contaminated with T. solium eggs. Yes [1–5] Drinking water contaminated with T. solium eggs. Yes [10] Yes [11] Yes [10] Caprid meat

Sources for Table A8.1.2: 1. (Reg.) Phiri, I.K., Ngowi, H., Afonso, S. and 16 others. 2003. The emergence of Taenia solium cysticercosis in Eastern and Southern Africa as a serious agricultural problem and public health risk. Acta Tropica, 87(1): 13–23. Krecek, R.C., Michael, L.M., Schantz, P.M., Ntanjana, L., Smith, M.F., Dorny, P., Harrison L.J.S., Grimm, F., Praet, N. & Willingham III, A.L. 2008. Prevalence of Taenia solium cysticercosis in swine from a community-based study in 21 villages of the Eastern Cape Province, South Africa. Veterinary Parasitology, 154(1-2): 38–47. Ekong, P.S., Juryit, R., Dika, N.M., Nguku, P. & Musenero, M. 2012. Prevalence and risk factors for zoonotic helminth infection among humans and animals - Jos, Nigeria, 2005–2009. The Pan African Medical Journal, 2012;12:6 [Online -- see http:/ /www.panafrican-med-journal.com/content/article/12/6/full/ ]. Ngowi, H.A., Kassuku, A.A., Maeda, G.E.M., Boa, M.E. & Willingham, A.L. 2004. A slaughter slab survey for extra-intestinal porcine helminth infections in northern Tanzania. Tropical Animal Health and Production, 36(4): 335–340. Knight-Jones, T.J.D., Mylrea, G.E. & Kahn, S. 2010. Animal production food safety: priority pathogens for standard setting by the World Organisation for Animal Health. Revue Scienti que et Technique OIE, 29(3): 523–535. Dorny, P., Phiri, I., Gabriel, S., Speybroeck, N. & Vercruysse, J. 2002. A seroepidemiological study of bovine cysticercosis in Zambia. Veterinary Parasitology, 104(3): 211–215. Tolosa, T., Tigre, W., Teka, G. & Dorny, P. 2009. Prevalence of bovine cysticercosis and hydatidosis in Jimma municipal abattoir, South West Ethiopia. Onderstepoort Journal of Veterinary Research, 76(3): 323–326. Ejima, I.A. & Uma, J.O. 2007. Taenia saginata (Goeze, 1782) in cattle slaughtered in Idah Metropolis, Kogi State, Nigeria. The Zoologist, 5: 8–15. Gajadhar, A.A., Scandrett, W.B. & Forbes, L.B. 2006. Overview of food- and waterborne zoonotic parasites at the farm level. Revue Scienti que et Technique de l’OIE, 25(2): 595–606. Elmahdi, I.E., Ali, Q.M., Magzoub, M.M.A., Ibrahim, A.M., Saad, M.B. & Romig, T. 2004. Cystic echinococcosis of livestock and humans in central Sudan. Annals of Tropical Medicine and Parasitology, 98(5) 473–479. Huttner, M., Siefert, L., Mackenstedt, U. & Romig, T. 2009. A survey of Echinococcus species in wild carnivores and livestock in East Africa. International Journal for Parasitology, 39(11): 1269–1276.

2. (Reg.)

3. (Reg.)

4. (Reg.)

5. (Global)

6. (Reg.)

7. (Reg.)

8. (Reg.) 9. (Global)

10. (Reg.)

11. (Reg.)

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A8.1.3 Agri-food trade Most of the above parasites have minor regional or global trade implications, except for T. solium, Trichinella spp. in pork and pork products, and T. saginata in beef and beef products, which do have trade implications. In most countries, carcasses may not be released even for the domestic market unless they have been inspected and/or tested to ascertain absence of infection.

A8.1.4 Consumer perception Because of lack of public awareness campaigns and education concerning the risks of eating certain foods, especially meat and meat products, in many African countries, consumers in Africa are ignorant of the prevalent of foodborne parasites. To some extent, consumers in some countries are aware of T. solium and saginata cysticercosis, but in some cases they are ignorant of the importance of meat inspection and hygiene. In some countries, consumers are aware of the e ects of hydatid cysts of Echinococcus granulosus but are ignorant of not how the parasite is transmitted. e risk of human infection from infected meat and vegetables is reduced by cooking, which destroys the pathogen, because of the reduced use of raw vegetables this has limited transmission.

A8.1.5 Social sensitivity Neurocysticercosis due to T. solium infection is one of the main causes of epilepsy in rural African communities. is comes with social stigma for those a ected by the parasite. Another disease that might have social sensitivity in the African context is congenital toxoplasmosis, which might cause abortions and foetal deformities, creating a variety of social problems within a community. e disease has substantial global impact in terms of disability adjusted life years (DALYs) and monetary losses. Furthermore, in most reports, between 1 and 2 hydatid cysts in humans are fatal, depending on their location, and the DALYs are substantial. T. solium, T. saginata and E. granulosus are considered to have economic impact when it comes to monetary loss due to carcass devaluation or condemnation, which is recognized by a lot of the people. is a ects not only human and animal health directly, but also agriculture in general.

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A8.1.6 Risk management TABLE A8.1.3 Data availability for risk management options for main parasite-commodity combinations in Africa. NOTE: The authors were asked to consider all combinations of the particular parasite and the main food categories, namely Beef, Dairy, Pork, Poultry, Game, Seafood, Fruit, Vegetables and Other.

Cryptosporidium spp. Beef Fruits Vegetables Other Yes [9] Yes [12, 13] Yes [12, 13] Yes [12, 13]

Echinococcus granulosus Beef Other Taenia solium Pork Other Taenia saginata Beef Pork Other Trichinella spiralis Pork Game Yes [7, 8] Yes [7, 8] Yes [6] Yes [5] Yes [5, 6] Yes [1–4] Yes [1–4] Yes [9–11]

Sources used for Table A8.1.3: 01. Sikasunge, C.S., Phiri, I.K., Phiri, A.M., Dorny, P., Siziya, S. & Willingham, A. L. III. 2007. Risk factors associated with porcine cysticercosis in selected districts of Eastern and Southern provinces of Zambia. Veterinary Parasitology, 143(1): 59–66. Mkupasi, E.M., Ngowi, H.A. & Nonga, H.E. 2011. Prevalence of extra-intestinal porcine helminth infections and assessment of sanitary conditions of pig slaughter slabs in Dar es Salaam city, Tanzania. Tropical Animal Health and Production, 43(2): 417–423. Krecek, R.C., Mohammed, H., Michael, L.M., Schantz, P.M., Ntanjana, L., Morey, L., Werre, S.R. & Willingham, A.L. III. 2012. Risk factors of porcine cysticercosis in the eastern Cape Province, South Africa. PLOS ONE, 7(5): Art. no. e37718 [Online]. Gweba, M., Faleke, O.O., Junaidu, A.U., Fabiyi, J.P. & Fajinmi, A.O. 2010. Some risk factors for Taenia solium cysticercosis in semi-intensively raised pigs in Zuru, Nigeria. Veterinaria Italiana, 46(1): 57–67. Cabaret, J., Geerts, S., Madeline, M., Ballandonne, C. & Barbier, D. 2002. The use of urban sewage sludge on pastures: the cysticercosis threat. Veterinary Research, 33(5): 575–597. Skjerve, E. 1999. Possible increase of human Taenia saginata infections through import of beef to Norway from a high prevalence area. Journal of Food Protection, 62(11): 1314– 1319.

02.

03.

04.

05.

06.

180

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07.

Theodoropoulos, G., Theodoropoulou, H., Skopelitis, G. & Benardis, K. 2009. Assessment of swine farms in Greece in relation to the risk of exposure of pigs to Trichinella. Preventive Veterinary Medicine, 89(3-4): 277–281. Alban, L., Boes, J., Kreiner, H., Petersen, J.V. & Willeberg, P. 2008. Towards a riskbased surveillance for Trichinella spp. in Danish pig production. Preventive Veterinary Medicine, 87(3-4): 340–357. Buishi, I.E., Njoroge, E.M., Bouamra, O. & Craig, P.S. 2005. Canine echinococcosis in northwest Libya: Assessment of coproantigen ELISA, and a survey of infection with analysis of risk-factors. Veterinary Parasitology, 130(3-4): 223–232. Takumi, K., Hegglin, D., Deplazes, P., Gottstein, B., Teunis, P. & Van Der Giessen, J. 2012. Mapping the increasing risk of human alveolar echinococcosis in Limburg, The Netherlands. Epidemiology and Infection, 140(5): 867–871. Pavlin, B.I., Schloegel, L.M. & Daszak, P. 2009. Risk of importing zoonotic diseases through wildlife trade, United States. Emerging Infectious Diseases, 15(11): 1721–1726. Kimani, V.N., Mitoko, G., McDermott, B., Grace, D., Ambia, J., Kiragu, M.W., Njehu, A.N., Sinja, J., Monda, J.G. & Kang’ethe, E.K. 2012. Social and gender determinants of risk of cryptosporidiosis, an emerging zoonosis, in Dagoretti, Nairobi, Kenya. Tropical Animal Health and Production, 44(Suppl. 1): S17–S23. Grace, D., Monda, J., Karanja, N., Randolph, T.F. & Kang’ethe, E.K. 2012. Participatory probabilistic assessment of the risk to human health associated with cryptosporidiosis from urban dairying in Dagoretti, Nairobi, Kenya. Tropical Animal Health and Production, 44(Suppl. 1): S33–S40.

08.

09.

10.

11. 12.

13.

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ANNEX 8.2 ASIA A8.2.1 Introduction Foodborne Parasitic diseases are widely distributed in south-east, east and south Asia, and have been major public health problem for the population in the countries and regions. Distribution and endemicity of individual foodborne parasitic diseases vary greatly among countries and regions. While a majority of foodborne parasitic diseases are restricted to a few countries, or even local areas, there are some diseases prevalent much more widely. is section tries to summarize the current status of foodborne parasitic diseases in Asia. e information for Asia was collected by Nguyen Van De, Viet Nam; Tomoyoshi Nozaki, Japan; Subhash Parija, India; and Paiboon Sithithaworn, ailand. One should note that some of statistics regarding endemicity were based on serology and/or microscopy, and thus potentially erroneous due to lack of proper objective diagnostic methods such as PCR and antigen detection of parasites, and confounded by potential cross-reactivity of sera from individuals infected with other parasites in tests using crude or unde ned antigens.

A8.2.2 Description of individual foodborne parasitic diseases e foodborne parasitic diseases are considered hierarchically as, rstly, meat-, sh-, shell sh- and plant-borne infections, secondly as protozoan and helminth infections, and thirdly in alphabetical order.

A8.2.2.1 Meat-borne parasite infections Sarcocystosis (intestinal) Intestinal sarcocystosis domestically is distributed in some countries, including China (29.7%), Malaysia (19.7% of 243 persons had antibodies to sarcocystis), India (11 case reports from 1990 to 2004), ailand (1.5%) and Japan (case reported). In Viet Nam none were reported. In Japan, a case that may be relevant to international trade has recently emerged. Sarcocystis infection through consumption of raw horse meat (“Basashi”) is becoming an important social health problem, with 37 clinical complaints related to consumption of fresh market horsemeat reported, mainly from the producing centres in Japan. e Sarcocystis species responsible for cases has been determined by rRNA sequencing to be closest to S. fayeri. Both horse meat imported unfrozen and live horses imported (mainly from North America) and raised in Japan were proven to be infected with the species at high possibility. Proper freezing (-20ºC for >48 hours) can eliminate live parasites. Toxoplasmosis Toxoplasmosis, caused by the protozoan parasite Toxoplasma gondii, is prevalent in

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Asia. However, data on most the serious form of toxoplasmosis, congenital toxoplasmosis, is largely unavailable. In China, the rst human case of toxoplasmosis was reported in 1964 in Jiangxi Province. Many human cases have been were reported in China since the rst epidemic survey on toxoplasmosis was carried out in Guangxi Province in 1978. Between 2001 and 2004, a national serological survey of 47 444 people in 15 provinces and autonomous regions estimated a mean prevalence of 7.9% by using enzyme-linked immunosorbent assay (ELISA). High seroprevalence of latent T. gondii infection has been found among immunocompromised patients. Prevalence of T. gondii infection in cancer patients ranged from 24% to 79%. Surveys of T. gondii infection in individuals with tuberculosis and hepatitis B showed that the prevalences were 35.3% and 19.3%, respectively. In India, in the general population, seropositivities were 10.8–51.8% for IgG and 2–5% for IgM. In females with a bad obstetric history IgG was 49.5%. In HIV-infected subjects, seropositivity for IgG was 70%. In ailand, the prevalence of toxoplasmosis was 2.6%. In Viet Nam, some cases of toxoplasmosis were reported. In Sri Lanka, the prevalence of toxoplasmosis was 27.5%. In Japan, the prevalence of toxoplasmosis was 1.8–5.6%. In Malaysia, the prevalence of toxoplasmosis was 10–50%. In Nepal, the prevalence of toxoplasmosis was 45.6%. In Viet Nam, some cases were reported. Food attribution to toxoplasmosis in Asia remains not well understood. Taeniasis/cysticercosis Human Taeniasis refers to foodborne infections with adult tapeworms: Taenia solium, Taenia asiatica (from pigs) or Taenia saginata (from cattle). Cysticercosis is a tissue infection with the larval cysticercus or metacestode stage of tapeworms, and occurs most commonly in pigs and cattle. e larval stage of Taenia solium can also infect humans and cause cysticercosis/neurocysticercosis, which is considered widespread in the developing countries of Latin America, Africa and Asia. In Viet Nam, the infection rate of Taenia (serology) was 0.5–2% in the plains area, 3.8% in the highlands and 2–6% in mountain areas. Most taeniasis was due to T. saginata and T. asiatica (78–80%) or T. solium (20–22%). Cysticercosis is distributed in many provinces (over than 50 provinces), the prevalence was 5–7% in some villages. In China, the emergence of cysticercosis as a serious public health problem was recognized by the Chinese Government. Human cysticercosis caused by the larval stage of T. solium occurred in 29 provinces/autonomous regions/municipalities, and about 7 million people were estimated to be infected. Currently, T. solium and cysticercosis are highly endemic, primarily in Yunnan, Sichuan and Guizhou in the south-west, and in Qinghai province and Inner Mongolia in the north-west and northern regions. In ailand, the prevalence of Taeniasis varies from 0.6 to 5.9%, and cysticercosis was 4% (based on serology). In Japan, 446 cystiANNEX 8 REGIONAL REPORTS

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cercosis cases were reported up to 2004. In the Philippines, the reported prevalence of Taeniasis varied greatly, from 0.56 to 10% and cases reported. Indonesia, the prevalence of Taenia was 8–9% and cases reported of cysticercosis. In Bangladesh, case reports identi ed Taenia spp. In Nepal, the prevalence of Taenia spp. was 43% and cases reported for cysticercosis. In India, the prevalence of T. solium (18.6%), prevalence of neurocysticercosis (NCC) in asymptomatic individuals (15.1%), prevalence of NCC in active epileptics (26.3–56.8%) and prevalence of T. saginata was 5.3%. Note that these statistics regarding endemicity were o en based on serology, and thus potentially erroneous due to cross-reactivity. In addition, as these infections occur mostly with domestically, but not internationally, traded meats, these diseases may not currently be a serious issue in Asia. Trichinellosis Trichinellosis in Asia is restricted to China and a few south-eastern countries. In China, more than 500 outbreaks in 12 of 34 provinces were reported, with 25 685 persons a ected and 241 deaths. In Viet Nam, 5 trichinellosis outbreaks were reported, in the province of Yen Bai in 1970, Dien Bien in 2002 and 2004, Son La in 2008 and anh Hoa in 2012, with 114 cases and 8 deaths in total. In ailand, the prevalence of trichinellosis was 0.9–9% (based on serology). In Japan, only one case was reported of trichinellosis. In India, there have been very few case reports, but recently a point source outbreak involved 42 cases. Note that these statistics regarding endemicity were mostly based on serology, and thus potentially erroneous due to cross-reactivity. In addition, as these infections occur mostly with domestically, but not internationally traded meats, these diseases may not currently be a serious issue in Asia.

A8.2.2.2 Fish- and shell sh-borne parasites Anisakiasis (including Pseudoterranova sp.) Anisakiasis is endemic in eastern Asian countries and regions, including Japan, Korea, mainland China and Taiwan. Due to the increasing popularity of Sushi and Sashimi, its worldwide distribution has potentially some relevance to the present FAO/WHO consultation. e worm species most commonly involved in human infections is Anisakis simplex. In Japan, 2 511 cases were reported between 2001 and 2005, and it is estimated—based on a survey using medical practitioners’ receipts for health insurance claims—that a few to several thousand cases occurred annually in Japan. Anisakiasis has not been reported in South-East and South Asian countries, including India, ailand and Viet Nam. e only cases reported of Pseudoterranova decipiense were from Japan and Taiwan. Capillariasis Capillaria philippinensis was reported in the Philippines, Japan, Indonesia and India, with 3 case reports up to 2012. 184 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

ailand, Taiwan,

Clonorchiasis e oriental liver uke, Clonorchis sinensis, is of socioeconomic importance in East and South-East Asia, including China, Taiwan, Viet Nam, Korea, and, to a lesser extent, in Japan. It is estimated that about 35 million people are infected globally, of whom approximately 15 million are in China in 27 provinces, which is a three-fold increase in the last decade. In Korea there have been 2 million infected, with a prevalence of 1.4–21.0%. In Japan, the prevalence was 1.0–54.2% (1960) and 10.9–66% (1961), but now has almost disappeared. In Viet Nam, the prevalence is 19.5% (0.2–40%) in 15 of 64 provinces in the north of the country. In Taiwan, prevalence is 10–20%. India has had very few cases reported. Note that these statistics regarding endemicity were very o en based on serology, and thus potentially erroneous due to cross-reactivity. In addition, as these infections occur mostly with domestically but not internationally traded meats, these diseases may not currently be a serious issue in Asia. Gnathostomiasis Gnathostomiasis is restricted to South-East Asian countries. Cases reported of Gnathostoma spp. include 40 cases in Japan (2000–2011), 86 in China, and 34 in other Asian countries. Cases have been reported in China, ailand, Viet Nam, India, Laos PDR, Myanmar, Cambodia, Bangladesh, Malaysia, Indonesia, Philippines and in India, with 14 cases reported up to 2012. Echinostomiasis Reported prevalences of Echinostoma spp. were 0.04–55.3% in ailand, 1.5–20.1% in China (based on serology), a single case in Viet Nam and a few cases in India. Kudoa infections Kudoa infections from consumption of unfrozen raw at sh (“Hirame”) have been reported only recently in Japan. However, the number of cases is growing since the identi cation and noti cation of the causative agent. By 2011, 33 incidents involving 473 cases had been reported, with outbreaks also common. Food poisoning associated with at sh consumption can be prevented by freezing at -20°C for 4 hours or heating at 90°C for 5 minutes, which inactivates Kudoa septempunctata. However, in view of the high market value of live at sh, the Fishery Agency is currently taking measures towards Kudoa-free at sh aquaculture. Currently, unfrozen at sh is consumed only in East Asia, including Japan and Korea, but Kudoa may have an impact on food trade when at sh consumption becomes more widely popular. Opisthorchiasis Opisthorchiasis is restricted to a few SE countries, where eating raw freshwater sh is common. In ailand, prevalence of opisthorchiasis was 15.7%. In Lao PDR, ANNEX 8 REGIONAL REPORTS

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the prevalence of opisthorchiasis was 37–86%. In Cambodia, opisthorchiasis was found in some cases. In Viet Nam, the prevalence of opisthorchiasis was 1.4–37.9% in 9/64 provinces in the south. In Malaysia, one case was reported of opisthorchiasis. In India, no cases have yet been reported. As opisthorchiasis occurs mostly in a domestic context, it is irrelevant to international trade in Asia. Paragonimiasis Paragonimus westermani has major socioeconomic importance in some restricted SE Asian countries and China. e parasite is transmitted via snails to freshwater crabs or cray sh, then to humans and other mammals, such as cats and dogs, and causes paragonimiasis. us, paragonimiasis is restricted to countries and regions where easting raw crab meat, which is locally distributed, is practised. In China, species of medical importance are Paragonimus westermani, P. szechuanensis, P. heterotremus, P. huetiungensis and P. skrjabini. P. westermani has been reported in humans from 24 provinces of mainland China, with a prevalence of 4.1–5.1%, with the population at risk of paragonimiasis being about 195 million. In Viet Nam, prevalence was 0.5–15% in 10/64 provinces based on serology. Adult worms found in dogs and infected cats, identi ed by morphology and molecular methods, were P. heterotremus. In ailand, cases were reported in 23/68 provinces. In Japan, over 200 cases have been reported, but only a few recent cases. In Philippines, prevalence was 27.2–40% by serology in some areas. In India, it is endemic to the northeastern states of Manipur, Nagaland and Arunachal Pradesh, where P. heterotremus is the common species, with up to 50% seroprevalence in these regions. Note that these statistics regarding endemicity were mostly based on serology and thus potentially erroneous due to cross-reactivity. In addition, as these infections occur mostly through domestically but not internationally traded meats, these diseases may not currently be a serious issue in Asia. Small intestinal ukes Small intestinal ukes reported included Heterophiydae (Haplorchis taichui, H. pumilio, H. yokogawai, Metagonimus spp, Centrocestus spp, Lecitodendriids) and Echinostomatidae (Echinostoma spp., Echinochasmus spp.). Many cases were reported of small intestinal ukes in Korea, with 19 species identi ed. In Viet Nam, small intestinal ukes were widely distributed with a high prevalence (over 50% in some endemic areas), with 6 species in humans. Flukes are common in ailand, with cases reported from China, Japan and India. Sparganosis A case was reported of Spirometra erinacei causing sparganosis in humans in Japan (an imported case), and Viet Nam and India have had few cases reported.

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A8.2.2.3 Plant (fruit and vegetable)-borne parasites Amoebiasis Entamoeba histolytica is widely distributed in Asia. For instance, in Viet Nam, prevalence is 2-6% in children; in India, intestinal amoebiasis with E. histolytica or E. dispar (1–58%), intestinal amoebiasis with proven E. histolytica (34.6% of all the samples found to be positive for E. histolytica or E. dispar), extra-intestinal amoebiasis – amoebic liver abscess (3–9% of all the cases of intestinal amoebiasis). In Japan, in contrast, E. histoltyica infections are restricted to faecal spread though anal intercourse or faecal smearing by persons with intellectual disabilities, and thus its impact on foodborne transmission of the disease is very limited. In addition, as its transmission is primarily local and domestic in all endemic countries and regions, amoebiasis may be irrelevant to international trade. Furthermore, as transmission occurs locally and domestically in all endemic countries and regions, amoebiasis is irrelevant to international trade. Cryptosporidiosis In Viet Nam, an infection rate of cryptosporidiosis was 2.8% reported on a national basis. In India, the infection rate of Cryptosporidiosis was 18.9% in children, who had diarrhoea. In Japan, no foodborne case of cryptosporidiosis has been reported. In China, the infection rate of Cryptosporidiosis was 1.36–13.3%. Note that some of these numbers may not be reliable. As its transmission occurs locally and domestically in all endemic countries and regions, cryptosporidiosis is probably irrelevant to international trade. In addition, the main route of transmission is drinking water, and food attribution is not well understood. Giardiasis Giardiasis is caused by Giardia duodenalis (syn. G. lamblia, G. intestinalis), which constitutes the most common intestinal protozoan worldwide. Contaminated water is an important source of human infection, either through direct consumption or through the use of contaminated water in food processing or preparation. Human infection with Giardia duodenalis has been documented in every province of mainland China. e infection rate ranged from 8.67% to 9.07%, which were extracted from 13 areas out of 35 cities at the provincial level. Giardiasis is more common in children (<10 years old), and the prevalence varied from 5.0% in children aged 5–9 years to 4.2% in children aged 10–14 years. In Viet Nam, the prevalence was 1–10%. In India, countrywide distribution was 8.4–53.8%. However, as its transmission is principally local and domestic in all endemic countries and regions, giardiasis is irrelevant to international trade. In addition, the main route of transmission is drinking water, and food attribution is not well understood.

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Ascariasis Ascariasis is among the most common helminth infections worldwide, including Asia. However, as its transmission is local and domestic in all endemic countries and regions, ascariasis is irrelevant to international trade. In China, a recent nationwide survey suggested that Ascaris lumbricoides infection was the most common helminthiasis, with an overall prevalence of 47% and an estimated 531 million infections, and was most prevalent in children between 5 and 19 years old. In Viet Nam, the prevalence of ascariasis in communities in most provinces was 10–95%, with the greatest endemic infection rates being 80–95% in the Red River delta region, and least in the south and highland regions (10–40%). In Japan, the prevalence of Ascariasis was 8.2% in 1956, and is currently very low. In India, countrywide it is the commonest intestinal helminth ((28.4–68.3%). However, since its transmission is local and domestic in all endemic countries and regions, ascariasis is irrelevant to international trade. Angiostrongyliasis Angiostrongyliasis caused by Angiostrongylus cantonensis is a potentially fatal parasitic disease. e biggest outbreak in China thus far could be attributed to a freshwater snail and took place in the capital Beijing in 2006. Of the 160 infected individuals involved in this outbreak, 100 were hospitalized. In ailand, case reports showed 484 cases from 1965 to 1968. In Viet Nam, over 60 cases were reported from many areas, most of them in children. In Japan, there have been 54 cases reported. In India, there is a single case report. Angiostrongyliasis is regionally restricted and irrelevant to international trade. Coenurosis Cerebral coenurosis or, more appropriately, central nervous system coenurosis (CNSc), is caused by infection with the larval stage (Coenurus cerebralis) of Taenia multiceps. is disease is very rare in humans and only about 100 cases have ever been recorded in China. Most human cases occur in developing countries, including India. Echinococcosis Echinococcosis, including cystic echinococcosis (CE) caused by the cestode Echinococcus granulosus and alveolar echinococcosis by E. multilocularis are regarded as among the most serious parasitic zoonoses. In China, the recent nationwide ELISA survey estimated that 380 000 people were infected with echinococcosis and ca. 50 million at risk of infection. In Japan, 373 cases (26 deaths) of alveolar echinococcosis were reported in 1997. Infection of wild foxes still persists, which may pose a public health risk for foodborne transmission of echinococcosis. Cases have been reported in South Korea, Mongolia, ailand, Bangladesh, Nepal and India. Despite the fact that food attribution of echinococcosis is not well under188 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

stood in Asia, it may have some relevance to international trade due to the severity of disease outcomes. Fasciolopsiasis Fasciolopsis buski is an intestinal trematode of humans and pigs that is acquired by consumption or handling of aquatic plants Fasciolopsiasis is restricted to some part of SE and East Asia, and irrelevant to international trade. In China, the rst national survey between 1988 and 1992 revealed that fasciolopsiasis was distributed across 16 provinces and a ected a total of 9531 infected people with 10.2– 92.9% in some areas. e prevalence of infection in children ranged from 57% in mainland China to 25% in Taiwan. In Viet Nam, the prevalence of fasciolopsiasis was 0.5–3.8% in 16/64 provinces. In ailand, its prevalence was 10% in children, who had intestinal parasites. Cases have been reported in Taiwan, Cambodia, Laos, Malaysia, Indonesia, Myanmar and India with a prevalence of 0–22.4%. Fascioliasis Fascioliasis is restricted to some part of SE Asia, and irrelevant to international trade. In Viet Nam, fascioliasis has been found in 52 of 63 provinces of the country, including 26 provinces in the south and 26 provinces in the north. Samples of Fasciola eggs and adult worms collected from the patients were analysed and identi ed by molecular methods as Fasciola gigantica. It is suggested that the Vietnamese F. gigantica has been hybridized with F. hepatica. In China, a national survey between 1988 and 1992 found 148 people were infected with F. hepatica and 9 with F. gigantica. Cases have been reported in ailand, Korea, Islamic Republic of Iran, Japan, Malaysia, Singapore, Laos, Cambodia, Philippines and India. Hookworm disease In Viet Nam, the hookworm infection rate of was 30–85% in the north and 47–68% in the south, most of them being Necator americanus (95–98% of cases). Country-wide distribution in India was 28.9–43%. Cases have been reported in China, Korea and Japan. Signi cance of foodborne transmission of hookworms in Asia is not known. Toxocariasis In India, it is endemic in the northern states, up to 33% in Kashmir and with seropositivity of 6–23% in other northern states. In Viet Nam, one case report indicated hundreds of cases. In Japan, some cases have been reported. Foodborne attribution is not known. Trichuriasis In Viet Nam, distribution of trichuriasis is as wide as ascariasis, with a prevalence rate of 0.5–89% in surveys, with the infection rate in the north higher than in the south. In ailand prevalence was 70%, and in Laos it was 41.5%. ANNEX 8 REGIONAL REPORTS

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A8.2.3 Risk management strategies e strategies for control of foodborne parasites are combination of the regulation of an entire food chain from production to consumption. ey also include creation of consumer perception and agri-food trade regulation. For some foodborne parasitic diseases, food habits of eating raw materials (e.g. freshwater sh) are the primary cause of endemicity and national, regional, and local activities to increase public awareness are essential. However, these diseases are mostly local and consequently not addressed as part of the meeting.

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TABLE A8.2.1 Data availability on the burden of disease and food attribution at the regional and global level for Asia Global level Disease severity/ main populations at risk Main food source and attribution Disease in humans Yes [92, 126–129] Vegetables, soil No data No data Disease severity/ Main food main sources and populations attributions at risk Vegetables, soil

Data availability on human disease related parameters

Regional level

Parasite species

Disease in humans

Yes [92, 126–129] Yes [127–129] Anaemia

Ancylostoma duodenale, Necator americanus

Viet Nam: – all country (3–85%)

China, Korea, Japan India – countrywide (28.9–43%) Yes [24, 121] Yes Snails, vegetables Yes

Yes [24, 121–123] Yes Snails/ vegetables

Angiostrongylus spp.

Thailand –484 cases reported from 1965 to 1968 China – 160 Cases reported in many areas Viet Nam – >60 cases reported in many areas Japan – 54 cases reported India – one case report No data Yes [79] Marine sh Yes [112, 144] Poor sanitation and hygiene Yes Diarrhoea, liver dysfunction Raw sh

Yes [79]

Anisakis simplex

Japan a case reported China – cases reported Not reported in India Yes [112, 144] Intestinal obstruction, mostly in children Yes [65]

No data

Yes Fish

Yes [59, 92, 112, 126, 128, 144]

Ascaris lumbricoides

Viet Nam – countrywide (5–95%) Japan – 8.2% in 1956 China – 47% India – countrywide (commonest intestinal helminth) – 28.4–68.3%

No data

Vegetables, food transmision

Yes [45, 65]

ANNEX 8 REGIONAL REPORTS

Capillaria philippinensis

Cases reported in Philippines, Japan, Thailand, Taiwan, Indonesia; India – 3 case reports till 2012

Fish

197

198 Global level Disease severity/ main populations at risk Main food source and attribution Disease in humans Disease severity/ Main food main sources and populations attributions at risk Yes [46, 48, 51, 52] Yes [48, 50] Yes [46, 47] Raw & undercooked sh. 601 million Acute disease Yes [46] 601 million Raw & undercooked sh (freshwater) Yes [92–94] No data [95] No data [91] No data [91] Yes [91] Water, vegetables HIV-related No data No data No data Vegetables, water raw meat (yukke) Yes [81–87] Yes [81, 82] Yes [66, 89] Yes [89] No data No data No data Yes Yes vegetables No data No data Vegetables Yes [73] Yes Raw snail & sh No data No data Yes Snail; sh

Data availability on human disease related parameters

Regional level

Parasite species

Disease in humans

Clonorchis sinensis

Yes [24, 46, 48–52] China – 15 million Korea – 2 million infected, prevalence of 1.4–21.0% Japan – prevalence of 1.0–54.2% (1960); 10.9–66% (1961); now almost disappeared Viet Nam – prevalence of 19.5% (0.2–40%) in 15/64 provinces in the north Taiwan – prevalence of 10–20% China – 15 million infected in 27 provinces India – Almost absent. Very few case reports

Yes [92, 95]

Cryptosporidium spp

Viet Nam – 2.8% and case reported (national) India – 18.9% in children with diarrhoea Japan – case reported China – 1.36–13.3%

Yes [81–87]

Diphyllobothrium spp.

Cases reported of D. nihonkaiense, D. latum, D. paci cum, D. cameroni, D. yonagoense in Japan Few cases of D. latum reported from south India

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Diplogonoporus balaenopterae

Yes [66, 89]

Case reported in Japan Not reported in India, Viet Nam or Thailand

Yes [59, 135–140]

Echinococcus spp.

Cases reported in Japan, China (380 000 cases), Korea, Mongolia, Thailand, Bangladesh, Nepal India – prevalence not clearly known; endemic in both rural and urban areas of southern and central states.

Yes [73–75]

Echinostoma spp

Japan – 22.4% Thailand – 0.04–55.3% China – 1.5–20.1% Viet Nam – a case reported India – very rare; very few case reports

Data availability on human disease related parameters Global level Disease severity/ main populations at risk Main food source and attribution Disease in humans Disease severity/ Main food main sources and populations attributions at risk

Regional level

Parasite species

Disease in humans

Yes [92, 148–152]

Entamoeba histolytica

Viet Nam – 2–6% in children India – intestinal amoebiasis with E. histolytica or E. dispar (1–58%); intestinal amoebiasis with proven Yes E. histolytica (34.6% of all samples found +ve E. histolytica or E. dispar); extra-intestinal amoebiasis – amoebic liver abscess (3–9% of all the cases of intestinal amoebiasis) No data No data Yes [111, 112] Yes Overcrowding No data

No data

Vegetables, water, food transmission

Yes [92, 111, 112, 157] No data

Enterobius vermicularis

Viet Nam – 29–43% in the north; 7.5–50% in the centre; 16–47% in the south; 51.2% in children 1–5 years old India – countrywide in children (0.5–12.6%); more common in rural than urban areas Yes [79, 92, 96] Water, raw vegetables

Yes [79, 92. 96, 99] Yes [79] No data No data water, vegetables

Fasciola spp

Viet Nam – >20 000 cases from 52/64 provinces Cases reported in China (148 cases), Thailand, Korea, No data Iran, Japan, Malaysia, Singapore, Laos, Cambodia & Philippines India – A few case reports Yes [102]

Yes [73, 92, 102, 103]

ANNEX 8 REGIONAL REPORTS

Fasciolopsis buski

Viet Nam – 0.5–3.8% in 16/64 provinces China – 10.2–92.9% in some areas Thailand – 10% in children with intestinal parasites Cases reported in Taiwan, Cambodia, Laos PDR, Malaysia, Indonesia & Myanmar India – endemic in E & NE states – prevalence of 0–22.4%

Yes [73, 92, 102] Abdominal pain, Water, raw diarrhoea, intestinal vegetables obstruction

No data

Water, raw vegetables

199

200 Global level Disease severity/ main populations at risk Main food source and attribution Disease in humans Disease severity/ Main food main sources and populations attributions at risk Yes [110, 154] No data No data No data Vegetables, water, food transmission Yes [71, 72] Ocular and cerebral manifestations Raw sh, amphibian reptile Yes [70] Fish, amphibian reptile Yes [53, 55] Yes [55]

Data availability on human disease related parameters

Regional level

Parasite species

Disease in humans

Yes [92, 110, 154]

Giardia duodenalis (syn. Viet Nam – 1–10% G. lamblia, G. intestinChina – infection rate ranged from 8.67%–9.07%, alis) found in 13 areas of 35 cities at the provincial level India – countrywide distribution (8.4–53.8%)

Yes [70–72, 90]

Gnathostoma spp

Cases reported in Japan with 3 225 cases, including 86 from China and 34 from other Asian sources. Cases reported in China, Thailand, Viet Nam, India, Laos PDR, Myanmar, Cambodia, Bangladesh, Malaysia, Indonesia and Philippines.

India – 14 cases reported until 2012

Yes [53–55] Raw sh dishes Yes [88] Yes Acute and selflimiting Yes Raw at sh (Paralichthys No data olivaceus) 100% foodborne transmission Yes [76, 78] Acute diarrhoea No data Fish; foodborne transmission Yes Yes Raw Fish

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Heterophyids

Thailand – 0.3–7.8% Viet Nam – 0.5–64.4% in >18 provinces China – 1–2% Japan – 11% India – Not yet reported

Kudoa septempunctata

No data

Not reported in India

Yes [57, 76, 78]

Metagonimus spp.

Many cases reported in Korea & China India – very rare. Very few case reports of Metagonimus yokogawai

Yes [76, 78] Undercooked No data freshwater sh

No data

Yes Fish

Regional level

Parasite species

Disease in humans

Yes [42, 44, 45] Yes [42, 44] Raw sh dish 10 million 67 million Yes [43] Yes [43]

Opisthorchis viverrini

Thailand – 15.7% Yes [42, 44] Lao PDR – 37–86% Cambodia – some cases 67 million Viet Nam – 1.4–37.9% in 9/64 provinces in the south. Malaysia – a case reported India – No cases yet reported. Yes [56, 60–62] Yes [60–62]

Yes [56–62] Raw crab; freshwater crab, wild boar meat in Japan Yes Yes

Paragonimus spp.

Thailand – cases reported in 23/68 provinces Viet Nam – 0.5–15% in 10/64 provinces Japan – case reports with >200 cases Philippines – 27.2–40% in some areas China – 4.1–5.1% in 24 provinces India – endemic to NE states (Manipur, Nagaland and Arunachal Pradesh); Paragonimus heterotremus is the common species; up to 50% seroprevalence in these regions. Cough, dyspnoea, recurrent haemoptysis No data Yes [79] Marine sh Yes [158] Raw horse meat 100% foodborne Acute and selflimited Yes [2,–4, 6] No data Meat (pork and beef) Raw pork muscle and o al

Freshwater crab; wild boar meat [56]

Yes [79]

Pseudoterranova decipiense Yes [158]

Case reported in Japan Not reported in India

No data

Yes Fish

Sarcocystis fayeri

Yes

Case reported in Japan [158]

Yes [1, 2, 4, 6] Yes No data No data Meat (pork and beef)

ANNEX 8 REGIONAL REPORTS

Sarcocystis spp.

Thailand (1.5%) India – 11 case reports from 1990 to 2004. A few earlier reports. China (29.7%) 46 cases reported by 1990 in Asia, including China, Malaysia and India. In Malaysia, 19.7% of 243 persons had antibodies to Sarcocystis

201

202 Global level Disease severity/ main populations at risk Main food source and attribution Disease in humans Yes [66–69] Abdominal, cerebral No data & ocular manifestations No data No data Frog Disease severity/ Main food main sources and populations attributions at risk Yes [13, 17] Yes [9] DALY: 2–5 ×106 Yes [9] Taeniasis – No NCC – Yes Epilepsy Meat (pork & beef) Beef, pork, pig viscera [9] Yes [133] Yes [133] Vegetables, food transmission No data No data Vegetables

Data availability on human disease related parameters

Regional level

Parasite species

Disease in humans

Spirometra erinaceieuropaei (sparganosis)

Yes [66–69]

Japan – case reported Viet Nam – case reported India – a few case reports

Yes [8, 10–19]

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Taenia spp.

Thailand – Taeniasis (0.6–5.9%) & cysticercosis (4%). Viet Nam – Taeniasis (0.5–12%) & cysticercosis (7%) in more than 50/64 provinces. Japan – cysticercosis 446 cases up to 2004. China – 7 million people infected in 29 provinces. Philippines – Taeniasis (0.56–10.26%) & case reported of cysticercosis. Indonesia – Taeniasis (0.56–10.26%) & case reported of cysticercosis. Bangladesh – case reported. Nepal – Taeniasis (43%) & case reported of cysticercosis. India – T. solium Taeniasis prevalence 18.6%; NCC prevalence in asymptomatic individuals 15.1%; NCC prevalence in active epileptics 26.3–56.8%; T. saginata Taeniasis prevalence 5.3%.

Yes [92, 126. 132, 133]

Toxocara spp.

Viet Nam – one case report Japan – one case report India – endemic in northern states; up to 33% in Kashmir; seropositivity of 6–23% in other northern states

Regional level

Parasite species

Disease in humans

Yes [30, 31, 33–41]

Yes [33, 36–38] CNS disease in HIV infected Yes [32]

Toxoplasma gondii

Thailand – 2.6% China – 12-45% and 12.7–15.1% Viet Nam – some cases reported Sri Lanka – 27.5% Japan – 1.8–5.6% Malaysia – 10–50% Nepal – 45.6% India – seropositivity for IgG in general population – 10.8–51.8% and for IgM – 2–5%; in females with bad obstetric history – IgG was 49.5%; in HIV-infected cases seropositivity for IgG 70%. Raw meat, pork, chicken, fruit, vegetables [30] Yes [32] Yes [21, 26, 27, 29] Yes [21, 26, 29]

Beef, pork, goat, horse, sheep, chicken; contaminated fruit & vegetables; raw mussels, clams & oysters

Yes [20–28]

Yes [21, 26, 29] Yes [21, 26, 29] Domestic pigs, wild boar, raw horse meat 100% foodborne transmission Yes [107]

Trichinella spiralis

Thailand – 0.9–9% Viet Nam – 5 outbreaks in north mountainous provinces, with >100 patients and 8 deaths up to Yes [25, 27] 2012. High mortality China – >500 outbreaks in 12/34 provinces, with 25 685 persons a ected (241 deaths). Japan – 1 case reported. India – very few case reports. Recently a point source outbreak of 42 cases. Yes Yes [106–109] Rectal prolapse

Meat; consumption of inadequately cooked wild boar meat

Yes [105, 108–112]

ANNEX 8 REGIONAL REPORTS

Trichuris trichiura

Thailand – 70% Laos PDR – 41.5% Viet Nam – 70–80% in the north and 5–10% in the south India – adults 2–6.6%; children 8–26.4%

Vegetable, personal hygiene

Yes

For 2010, global population at risk: 5023.3 (millions)

Foodborne

203

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008.

009. 010.

011.

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013. 014. 015. 016.

017. 018.

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020. 021.

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023.

024. 025.

026. 027. 028.

029. 030.

031. 032. 033. 036. 037.

038.

039.

040.

041. 042.

043.

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050. 051. 052. 053. 054.

055.

056. 057.

058.

059.

060. 061.

062. 065.

066.

067.

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MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

123.

Malhotra, S., Mehta, D.K., Arora, R., Chauhan, D., Ray, S. & Jain, M. 2006. Ocular angiostrongyliasis in a child – First case report from India. Journal of Tropical Pediatrics, 52(3): 223–225. Miyazaki, I. 1991. Helminthic zoonoses. SEAMIC publication, no. 62. International Medical Foundation of Japan, Tokyo. 494 p. Parija, S.C., Malini, G. & Rao, R.S. 1992. Prevalence of hookworm species in Pondicherry, India. Tropical and Geographical Medicine, 44(4): 378–380. Ragunathan, L., Kalivaradhan, S.K., Ramadass, S., Nagaraj, M. & Ramesh, K. 2010. Helminthic infections in school children in Puducherry, south India. Journal of Microbiology Immunology and Infection, 43(3): 228–232. Traub, R.J., Robertson, I.D., Irwin, P., Mencke, N. & Thompson, R.C.A. 2004. The prevalence, intensities and risk factors associated with geohelminth infection in tea-growing communities of Assam, India. Tropical Medicine & International Health, 9(6): 688–701. Fomda, B.A., Ahmad, Z., Khan, N.N., Tanveer, S. & Wani, S.A. 2007. Ocular toxocariasis in a child: A case report from Kashmir, north India. Indian Journal of Medical Microbiology, 25(4): 411–412. Malla, N., Aggarwal, A.K. & Mahajan, R.C. 2002. A serological study of human toxocariasis in north India. National Medical Journal of India, 15(3): 145–147. Parija, S.C., Rao, R.S., Badrinath, S. & Sengupta, D.N. 1983. Hydatid disease in Pondicherry. Journal of Tropical Medicine and Hygiene, 86(3): 113–115. Parija, S.C., Sasikala, A. & Rao, R.S. 1987. Serological survey of hydatid disease in Pondicherry, India. Transactions of the Royal Society of Tropical Medicine and Hygiene, 81(5): 802–803. Parija, S.C. 1991. Recent trends in serodiagnosis of hydatid disease. Review. Southeast Asian Journal of Tropical Medicine and Public Health, 22(suppl.): 371–376. Rao, S.S., Mehra, B., & Narang, R. 2012. The spectrum of hydatid disease in rural central India: An 11-year experience. Annals of Tropical Medicine and Public Health, 5(3): 225–230. Wani, S.A., Ahmad, F., Zargar, S.A., Ahmad, Z., Ahmad, P. & Tak, H. 2007. Prevalence of intestinal parasites and associated risk factors among schoolchildren in Srinagar City, Kashmir, India. Journal of Parasitology, 93(6): 1541–1543. Parija, S.C. & Rao, S. 1992. Serological survey of amoebiasis in Pondicherry. Indian Journal of Parasitology, 16(1): 69–72. Parija S.C. 2002. Epidemiology, clinical features and laboratory diagnosis of amoebiasis in India. Journal of Parasitic Diseases, 26(1): 1–8. Parija, S.C. & Khairnar, K. 2005. Entamoeba moshkovskii and Entamoeba disparassociated infections in Pondicherry, India. Journal of Health Population and Nutrition, 23(3): 292–295. Khairnar, K.S. & Parija, S.C. 2007. A novel nested multiplex polymerase chain reaction (PCR) assay for di erential detection of Entamoeba histolytica, E. moshkovskii and E. dispar DNA in stool samples. BMC Microbiology, 7: Art. No. 47 [Online] Parija, S.C. & Khairnar, K. 2008. Mutation detection analysis of a region of 16S-like ribosomal RNA gene of Entamoeba histolytica, Entamoeba dispar and Entamoeba moshkovskii. BMC Infectious Diseases, 8: Art. no. 131. [Online] Mirdha, B.R. & Samantray, J.C. 2002. Hymenolepis nana: A common cause of paediatric diarrhoea in urban slum dwellers in India. Journal of Tropical Pediatrics, 48(6): 331–334. Parija, S.C., Basile, A.L. & Nalni, P. 1999. Enterobius vermicularis infection in children in Pondicherry. Biomedicine, 19(2): 103–105. NIID (National Institute of Infectious Diseases, Japan). 2012. Kudoa and Sarcocystis food poisoning in Japan. IASR – Infectious Agents Surveillance Report, 33(6): 147–148. (IASR No. 388).

126. 127. 128.

129.

132.

133. 137. 138.

139. 140.

144.

148. 149 150.

151.

152.

154. 157. 158.

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209

TABLE A8.2.2 Data availability for parasite prevalence or concentration in the main food categories for Asia NOTE: Please read table in close association with Table A8.2.1. Game could include sh as sources are unclear.

Ancylostoma duodenale, Necator americanus Game Yes. Viet Nam – country-wide (3–85%); China, Korea, Japan. Vegetables Yes Other Yes [22] Vegetables, soils contact, walking barefoot on soil. Angiostrongylus spp. Game Yes. Thailand – 484 cases from 1965 to 1968; China – cases reported in many areas; Viet Nam – >50 cases in many areas; Japan – event reported with 54 cases. Other Yes [13] Snails, vegetables, raw frogs. Anisakis simplex Beef Yes [17] Pork Yes [17] Game Yes. Case reported. Other Yes. Marine sh. Ascaris lumbricoides Game Yes. Viet Nam – country-wide (5–95%); Japan – 8.2% in 1956. Vegetables Yes. Vegetables, improperly washed vegetables. Other Yes [24, 25] Vegetables, food transmision. Capillaria philippinensis Game Yes. Cases reported in Philippines, Japan, Thailand, Taiwan, Indonesia. Other Fish [14] Undercooked freshwater sh. Clonorchis sinensis Game Yes. China – 35 million; Korea – 2 million infected, prevalence of 1.4–21.0%; Japan – prevalence of 1.0–54.2% (1960) & 10.9–66% (1961); Viet Nam – prevalence of 19.5% (0.2–40%) in 15/64 provinces in the north; Taiwan – prevalence of 10–20%. Other Yes [3, 4] Fish. Cryptosporidium spp. Pork Yes. Game Yes. Viet Nam – 2.8% prevalence and case reported (national); India – 18.9% found in children with; Japan – case reported. Fruits Yes [8] Vegetables Yes [8] Grown in contact with soil Other Yes [8] Water; vetgetables; HIV-related. Water contaminated with human & animal excreta. Echinococcus spp. Game Yes. Cases reported in Japan, China, Korea, Mongolia, Thailand, Bangladesh, Nepal, India Vegetables Yes. Vegetables, but very little data. Other Yes [28] Vegetables, water and food contaminated with infected dog faeces, ngers as fomites on contact with dogs.

210

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Echinostoma spp. Game Yes. Japan – 22.4%; Thailand – 0.04–55.3%; China – 1.5–20.1%; Japan – 22.4%. Other Yes [18] Undercooked snails & freshwater sh. Entamoeba histolytica Game Yes. Viet Nam – 2-6% in children. Vegetables Yes [26] Improperly washed vegetables. Other Yes [26] Food transmision, food contaminated with human faeces. Fasciola spp. Pork Yes. Water, raw vegetables. Game Yes. Viet Nam – >20 000 cases from 52/64 provinces; Cases reported in China, Thailand, Korea, Iran, Japan, Malaysia, Singapore, Laos, Cambodia, Philippines. Vegetables Yes. Vegetables. Other Yes [20] Water, vegetables, aquatic plants, watercress. Fasciolopsis buski Dairy Yes Game Viet Nam – 0.5–3.8% in 16/64 provinces; China – 10.2–92.9% in some areas; Thailand: 10% in children with intestinal parasites; Cases reported in Taiwan, Cambodia, Laos, Malaysia, Indonesia, Myanmar, India. Vegetables Yes. vegetables; vegetables from aquatic plants. Other Yes [21] Water, vegetables, aquatic vegetation. Giardia duodenalis (syn. G. lamblia, G. intestinalis) Game Yes. Viet Nam – 1–10%. Vegetables Yes [27] Vegetables, improperly washed vegetables. Other Yes [27] Vegetables, food transmision, food contaminated with human faeces. Gnathostoma spp. Game Yes. Case reports from Japan (3225 cases including 86 in China and 34 in other Asian areas); Cases reported in China, Thailand, Viet Nam, India, Laos PDR, Myanmar, Cambodia, Bangladesh, Malaysia, Indonesia, Philippines. Other Fish & amphibian reptiles. [16] Raw or undercooked freshwater sh, amphibians, birds and mammals. Heterophyids Game Yes. Thailand – 0.3–7.8%; Viet Nam – 0.5–64.4% in >18 provinces; China – 1–2%; Japan – 11%. Other Yes. Fish. Metagonimus spp. Game Cases reported in Korea and Japan. Other Yes [19] Fish, undercooked freshwater sh. Opisthorchis viverrini Game Thailand – 15.7%; Lao PDR – 37–86%; Cambodia – some cases; Viet Nam – 1.4–37.9% in 9/64 provinces in south. Other Yes. Fish.

ANNEX 8 REGIONAL REPORTS

211

Paragonimus spp. Game Yes. Thailand – reported in 23/68 provinces; Viet Nam – 0.5–15% in 10/64 provinces; Japan – >200 cases reported; Philippines – 27.2–40% in some areas. Other Yes [9] Raw freshwater crab. Almost all Potamiscus manipurensis crabs found in streams in Nagaland contained metacercariae. Sarcocystis spp. Beef Yes [6] Pork Yes [7] Raw muscle and o al. Game Yes. Thailand – 1.5%. Other Yes [6, 7] Meat (pork, beef); wild boar. Spirometra erinaceieuropaei Beef Yes. Japan – case reported; Viet Nam – case reported. Other Frog [15] Drinking water with infected copepods; raw frog. Taenia spp. Beef Yes. Pork Yes [5] 7–20% of slaughtered pigs have cysticerci in their muscles. Game Yes. Thailand – 06–3.4%; Viet Nam – 0.5–12% in >50/64 provinces. Vegetables Improperly washed vegetables eaten raw in salads. Other Yes. Pork, beef. Toxoplasma gondii Beef Yes [11, 12] Dairy Yes [11, 12] Pork Yes [11, 12] Raw pork. Poultry Yes [11, 12] Game Yes. Thailand – 2.6%; China – 12–45%; Viet Nam – some cases reported; Sri Lanka – 27.5%; Japan – 1.8–5.6%; Malaysia – 10–50%; Nepal – 45.6%. Other Yes. Beef, pork, goat, horse, sheep, chicken; contaminated fruit, vegetables; raw mussels, clams, oysters. Trichinella spiralis Beef Yes [1] Pork Yes. Raw or undercooked. Game Thailand – 0.9–9%; Viet Nam – 5 outbreaks with over 100 cases (8 deaths); China – >500 outbreaks in 12/34 provinces, with 25 685 persons a ected (241 deaths). Other Yes [2] Under-cooked wild boar meat. Trichuris trichiura Game Yes. Vegetables, personal hygiene. Other Yes [10] Drinking water contaminated with human faeces. Toxocara spp. Game Yes. Viet Nam – case reported; Japan – case reported. Vegetables Yes. Vegetables, improperly washed vegetables. Other Yes [23] Vegetables, food transmision.

212

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Sources used for Table A8.2.2, but read in conjunction with references cited in the main text and in Table A8.2.1 01. Pebam, S., Goni, V., Patel, S. Kumar, V., Rawall, S. & Bali, K. 2012. Case Report: A 12-yearold child with trichinellosis, pyomyositis and secondary osteomyelitis. Journal of Global Infectious Diseases, 4(1): 84–88. Sethi, B., Butola, K.S., Kumar, Y. & Mishra, J.P. 2012. Multiple outbreaks of trichinellosis with high mortality rate. Tropical Doctor, 42(4): 243–243. De, N.V., Murrell, K.D., Cong, le D., Cam, P.D., Chau, le V., Toan, N.D. & Dalsgaard, A. 2003. The foodborne trematode zoonoses of Viet Nam. Southeast Asian Journal of Tropical Medicine and Public Health, 34(Suppl.1): 12–34. Mirdha, B.R., Gulati, S., Sarkar, T. & Samantray, J.C. 1998 Acute clonorchiasis in a child. Indian Journal of Gastroenterology, 17(4): 155. Prasad, K.N., Prasad, A., Verma, A. & Singh, A.K. 2008. Human cysticercosis and Indian scenario: a review. Journal of Biosciences, 33(4): 571–582. Nichpanit, S., Nakai, W., Wongsaroj, T. & Nithikathkul, C. 2010. First large scale of human Sarcocystis hominis in Thailand. Trends Research in Science and Technology, 2(1): 1–5. Banerjee, P.S., Bhatia, B.B. & Pandit, B.A. 1994. Sarcocystis suihominis infection in human beings in India. Journal of Veterinary Parasitology, 8(1): 57–58. Parija, S.C. 2000. Rare intestinal protozoal infections in India. Journal of International Medical Sciences Academy, 13(1): 49–54. Singh, T.S., Sugiyama, H., Umehara, A., Hiese, S. & Khalo, K. 2009. Paragonimus heterotremus infection in Nagaland: A new focus of paragonimiasis in India. Indian Journal of Medical Microbiology, 27(2): 123–127. Narain, K., Rajguru, S.K. & Mahanta, J. 2000. Prevalence of Trichuris trichiura in relation to socio-economic & behavioural determinants of exposure to infection in rural Assam. Indian Journal of Medical Research, 112: 140–146. Shivaprakash. M.R., Parija, S.C. & Sujatha, S. 2001. Seroprevalence of toxoplasmosis in HIV infected patients in Pondicherry. Journal of Communicable Diseases, 33(3): 221–223. Borkakoty, B.J., Borthakur, A.K. & Gohain, M. 2007. Prevalence of Toxoplasma gondii infection amongst pregnant women in Assam, India. Indian Journal of Medical Microbiology, 25(4): 431–432. Malhotra, S., Mehta, D.K., Arora, R., Chauhan, D., Ray, S. & Jain, M. 2006. Ocular angiostrongyliasis in a child – First case report from India. Journal of Tropical Pediatrics, 52(3): 223–225. Vasantha, P.L., Girish, N, & Sai Leela, K. 2012. Human intestinal capillariasis: A rare case report from non-endemic area (Andhra Pradesh, India). Indian Journal of Medical Microbiology, 30(2) 236–239. Sundaram, C., Prasad, V.S.S.V. & Reddy, J.J.M. 2003. Cerebral sparganosis. Journal of the Association of Physicians of India, 51(11): 1107–1109. Pillai, G.S., Kumar, A., Radhakrishnan, N., Maniyelil, J., Sha , T., Dinesh, K.R. & Karim, S. 2102. Case Report: Intraocular gnathostomiasis: report of a case and review of literature. American Journal of Tropical Medicine and Hygiene, 86(4):620–623. Ishikura, H. 2003. Anisakiasis (2) Clinical Pathology and Epidemiology. pp. 451–473, in: M. Otsuru, S. Kamegai and S. Hayashi (editors). Progress of Medical Parasitology in Japan, Vol. 8. Meguro Parasitological Museum, Tokyo, Japan. Grover, M., Dutta, R., Kumar, R., Aneja, S. & Mehta, G. 1998. Echinostoma iliocanum infection. Case report. Indian Pediatrics, 35 (June): 549–552. Uppal, B. & Wadhwa, V. 2005. Rare case of Metagonimus yokogawai. Indian Journal of Medical Microbiology, 23(1): 61–62. Ramachandran, J., Ajjampur, S.S.R., Chandramohan, A. & Varghese, G.M. 2012. Cases of human fascioliasis in India: Tip of the iceberg. Journal Of Postgraduate Medicine, 58(2): 150– 152.

02. 03.

04. 05. 06. 07. 08. 09.

10.

11. 12.

13.

14.

15. 16.

17.

18. 19. 20.

ANNEX 8 REGIONAL REPORTS

213

21.

Muralidhar, S., Srivastava, L., Aggarwal, P., Jain, N. & Sharma D.K. 2000. Fasciolopsiasis-a persisting problem in eastern U.P. – a case report. Indian Journal of Pathology and Microbiology, 43(1) 69–71. Parija, S.C., Malini, G. & Rao, R.S. 1992. Prevalence of hookworm species in Pondicherry, India. Tropical and Geographical Medicine, 44(4): 378–380. Malla, N., Aggarwal, A.K. & Mahajan, R.C. 2002. A serological study of human toxocariasis in north India. National Medical Journal of India, 15(3): 145–147. Wani, S.A., Ahmad, E., Zargar, S.A., Dar, P.A., Dar, Z.A. & Jan, T.R. 2008. Intestinal helminths in a population of children from the Kashmir valley, India. Journal of Helminthology, 82(4): 313–317. Ragunathan, L., Kalivaradhan, S.K., Ramadass, S., Nagaraj, M. & Ramesh, K. 2010. Helminthic infections in school children in Puducherry, south India. Journal of Microbiology Immunology and Infection, 43(3): 228–232. Parija S.C. 2002. Epidemiology, clinical features and laboratory diagnosis of amoebiasis in India. Journal of Parasitic Diseases, 26(1): 1–8. Parija, S.C. & Rao, R.S. 1987. Prevalence of parasitic infections in Pondicherry. Indian Journal of Parasitology,11: 63–65. Parija, S.C., Rao, R.S., Badrinath, S. & Sengupta, D.N. 1983. Hydatid disease in Pondicherry. Journal of Tropical Medicine and Hygiene, 86(3): 113–115.

22. 23. 24.

25.

26. 27. 28.

TABLE A8.2.3 Data availability for risk management options for each parasite-commodity combination in the Asia context. NOTE: The authors were asked to consider all combinations of the particular parasite and the main food categories, namely Beef, Dairy, Pork, Poultry, Game, Seafood, Fruit, Vegetables and Other.

Angiostrongylus spp. Other Yes [18] Proper cooking of frogs and snails Ancylostoma duodenale, Necator americanus Other Yes [28] Hookworm larvae were in areas 2.1–5.2% on vegetables. Vegetables & food transmission, so use sanitary disposal of human excreta; avoid walking barefoot. Anisakis simplex All No substantive data found. Ascaris lumbricoides Vegetables Yes. Ascaris eggs were in areas reported as 2.1–2.7% in vegetables. Other Yes [30] Vegetables & food transmission; hand washing; washing of vegetables before consumption; proper sanitation. Capillaria philippinensis Other Yes [19] Proper cooking of freshwater sh. Clonorchis sinensis Dairy Very little data [4] Game Yes [4] Viet Nam – 44.4–92.9% freshwater sh infected by Clonorchis sinensis larvae. Other Yes. Proper cooking of freshwater sh. Cryptosporidium spp. Beef Yes [11] Other Yes. Vegetables, food, water transmission; hand washing, boiling or ltration of drinking water Echinococcus spp. [34]

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MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Yes. Yes [34] Proper care of pet dogs; avoid close contact with stray dogs; hand washing; thorough washing of vegetables before consumption. Echinostoma spp. [23] Other Proper cooking of freshwater snails. Fasciola spp. Other Yes [25, 26] Fasciola larvae in areas reportedly 0.4% in vegetables. Avoid eating uncleaned aquatic plants and vegetables. Fasciolopsis buski Other Yes [27] Avoid eating uncleaned aquatic plants and vegetables. Entamoeba histolytica Game Yes. Vegetables Yes. E. histolytica cysts in areas reportedly 1.8–6.7% in vegetables. Other Yes [31] Vegetables & food; water transmission; hand washing; thorough washing of vegetables before consumption; proper sanitation. Giardia duodenalis (syn. G. lamblia, G. intestinalis) Game Yes. Vegetables Yes. Giardia cysts were in areas reportedly 2.7–13.9% in vegetables. Other Yes [32, 33] Vegetables & food; water transmission; hand washing; thorough washing of vegetables before consumption; proper sanitation. Gnathostoma spp. Game Yes. Gnathostoma larvae were in areas reportedly 6.7–11.4% in eels. Other Yes [22] Fish, eel, amphibians. Proper cooking of freshwater sh & frogs. Heterophyids Game Yes [12] Heterophyid larvae 7.4–62.8% in various sh species. Other Yes. Fish. Metagonimus spp. Other Yes [24] Proper cooking of freshwater sh. Opisthorchis viverrini Game Yes [4] Viet Nam – 10–29% freshwater sh infected by O. viverrini. Other Yes. Fish. Paragonimus spp. [13] Pork Yes. Wild boar meat. Game Viet Nam – rate of Paragonimus larvae was 9.7% to 98.1% in Potamicus crab. Other Yes [14] Freshwater crab, wild boar meat – proper cooking of crabs. Sarcocystis spp. Pork Yes [9] Proper cooking. Other Yes. Proper cooking of wild boar meat. Spirometra erinaceieuropaei Game Yes. 8–10% frogs reportedlt infected by S. erinaceieuropaei larvae. Other Yes [21] Frogs & amphibians; boiling or ltration of drinking water; Yes [17] Proper cooking. Proper cooking of frogs Taenia spp. [6] Beef Yes [7, 8] Discard infected meat in abattoir; proper cooking.

Vegetables Other

ANNEX 8 REGIONAL REPORTS

215

Pork Yes. Discard infected meat in abattoir; proper cooking. Game Yes. Viet Nam – 0.02–0.9% of pigs infected by T. solium larvae. Vegetables Yes. Proper washing before eating raw. Other Yes. Pork, beef. Toxocara spp. [15] Vegetables Yes [29] Other Thorough washing of vegetables before consumption. Toxoplasma gondii Beef Yes [17] Proper cooking. Dairy Yes [17] Proper cooking. Pork Yes [17] Proper cooking. Poultry Yes [17] Proper cooking. Trichinella spiralis Pork Yes. Proper cooking Game Yes [1, 2] Viet Nam – 70–879 Trichinella larvae per gram pork; China – 0.06%–5.6% infected in pigs, 16.2% in dogs, 0.7% in cattle and 0.8% in sheep. Other Yes [3] Livestock meat – proper cooking. Trichuris trichiura [15] Game The rate of Trichuris eggs in vegetable was 1.8–2.4%. Other Yes [16] Vegetables, food transmission. Pit latrines and potable drinking water would reduce prevalence. Sources consulted for Table A8.2.3 01. 02. 03. 04. 05. 06. 07. 08. De, N.V. Viet Nam. pp. 37–42, in: [Proceedings of the ] Seminar on Food- and Water-borne Parasitic Zoonoses (5thFBPZ), 28-30 November 2006, Bangkok, Thailand. Wang, Z.Q., Cui, J. & Shen, L.J. 2007. The epidemiology of animal trichinellosis in China. Veterinary Journal, 173(2)391–398. Sethi, B., Butola, K.S., Kumar, Y. & Mishra, J.P. 2012. Multiple outbreaks of trichinellosis with high mortality rate. Tropical Doctor, 42(4): 243–243. De, N.V. 2004. Fish-borne trematodes in Viet Nam. Southeast Asian Journal of Tropical Medicine and Public Health, 35(Suppl. 1): 299–301. Mirdha, B.R., Gulati, S., Sarkar, T. & Samantray, J.C. 1998 Acute clonorchiasis in a child. Indian Journal of Gastroenterology, 17(4): 155. De, N.V. and Le. 2010. Taenia/cysticercosis and molecular application. Scienti c Book. Medical Publish House, Viet Nam, 318 p. See pages: 66–67. Parija, S.C. & Sahu, P.S. A serological study of human cysticercosis in Pondicherry, South India. Journal of Communicable Diseases, 35(4): 283–289. Prasad, K.N., Prasad, A., Gupta, R.K., Pandey, C.M. & Singh, U. 2007. Prevalence and associated risk factors of Taenia solium taeniasis in a rural pig farming community of north India. Transactions of the Royal Society of Tropical Medicine and Hygiene, 101(12): 1241–1247. Banerjee, P.S., Bhatia, B.B. & Pandit, B.A. 1994. Sarcocystis suihominis infection in human beings in India. Journal of Veterinary Parasitology, 8(1): 57–58. Parija, S.C. Lalmuanpuii, J., Shiva Prakash, M.R. & Sheela Devi, C. 2001. Cryptosporidium, Isospora and Cyclospora infections in Pondicherry. Journal of Parasitic Diseases, 25(2): 61– 64. Chi, T.T.K., Dalsgaard, A., Turnbull, J.F. Tuan, P.A. & Murrell, K.D. 2008. Prevalence of zoonotic trematodes in sh from a Vietnamese sh-farming community. Journal of Parasitology, 94(2): 423–428.

09. 11.

12.

216

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

13. 14. 15. 16.

De, N.V. 2004. Epidemiology, pathology and treatment of paragonimiasis in Viet Nam. Southeast Asian Journal of Tropical Medicine and Public Health, 35(Suppl. 1): 331–336. Mahajan, R.C. 2005. Paragonimiasis: an emerging public health problem in India. Indian Journal of Medical Research, 121(6): 716–718. Phuong et al. 2011. Parasitic infection in wastewater-irrigated vegetables in rural and urban areas in Nam Dinh province. Journal of Military Medicine, 9 Nov. 2009: 33-37 Narain, K., Rajguru, S.K. & Mahanta, J. 2000. Prevalence of Trichuris trichiura in relation to socio-economic & behavioural determinants of exposure to infection in rural Assam. Indian Journal of Medical Research, 112: 140–146. Borkakoty, B.J., Borthakur, A.K. & Gohain, M. 2007. Prevalence of Toxoplasma gondii infection amongst pregnant women in Assam, India. Indian Journal of Medical Microbiology, 25(4): 431–432. Malhotra, S., Mehta, D.K., Arora, R., Chauhan, D., Ray, S. & Jain, M. 2006. Ocular angiostrongyliasis in a child – First case report from India. Journal of Tropical Pediatrics, 52(3): 223–225. Vasantha, P.L., Girish, N, & Sai Leela, K. 2012. Human intestinal capillariasis: A rare case report from non-endemic area (Andhra Pradesh, India). Indian Journal of Medical Microbiology, 30(2) 236–239. Sundaram, C., Prasad, V.S.S.V. & Reddy, J.J.M. 2003. Cerebral sparganosis. Journal of the Association of Physicians of India, 51(11): 1107–1109. Pillai, G.S., Kumar, A., Radhakrishnan, N., Maniyelil, J., Sha , T., Dinesh, K.R. & Karim, S. 2102. Case Report: Intraocular gnathostomiasis: report of a case and review of literature. American Journal of Tropical Medicine and Hygiene, 86(4):620–623. Grover, M., Dutta, R., Kumar, R., Aneja, S. & Mehta, G. 1998. Echinostoma iliocanum infection. Case report. Indian Pediatrics, 35 (June): 549–552. Uppal, B. & Wadhwa, V. 2005. Rare case of Metagonimus yokogawai. Indian Journal of Medical Microbiology, 23(1): 61–62. De, N.V. 2012. Fascioliasis in Viet Nam. Pers. comm. in response to request for data. Ramachandran, J., Ajjampur, S.S.R., Chandramohan, A. & Varghese, G.M. 2012. Cases of human fascioliasis in India: Tip of the iceberg. Journal Of Postgraduate Medicine, 58(2): 150– 152. Muralidhar, S., Srivastava, L., Aggarwal, P., Jain, N. & Sharma D.K. 2000. Fasciolopsiasis-a persisting problem in eastern U.P. – a case report. Indian Journal of Pathology and Microbiology, 43(1) 69–71. Parija, S.C., Malini, G. & Rao, R.S. 1992. Prevalence of hookworm species in Pondicherry, India. Tropical and Geographical Medicine, 44(4): 378–380. Malla, N., Aggarwal, A.K. & Mahajan, R.C. 2002. A serological study of human toxocariasis in north India. National Medical Journal of India, 15(3): 145–147. Wani, S.A., Ahmad, F., Zargar, S.A., Ahmad, Z., Ahmad, P. & Tak, H. 2007. Prevalence of intestinal parasites and associated risk factors among schoolchildren in Srinagar City, Kashmir, India. Journal of Parasitology, 93(6): 1541–1543. Parija, S.C. & Rao, R.S. 1987. Prevalence of parasitic infections in Pondicherry. Indian Journal of Parasitology,11: 63–65. Kang, G., Mathew, M.S., Rajan, D.P., Daniel, J.D., Mathan, M.M. & Muliyil, J.P. 1998. Prevalence of intestinal parasites in rural Southern Indians. Tropical Medicine & International Health, 3(1): 70–75. Parija, S.C., Rao, R.S., Badrinath, S. & Sengupta, D.N. 1983. Hydatid disease in Pondicherry. Journal of Tropical Medicine and Hygiene, 86(3): 113–115.

17.

18.

19.

21. 22.

23. 24. 25. 26.

27.

28. 29. 30.

32. 33.

34.

ANNEX 8 REGIONAL REPORTS

217

ANNEX 8.3 AUSTRALIA A8.3.1 Preparation e information for Australia was compiled by Dr Rebecca Traub, Senior Lecturer in Veterinary Public Health, School of Veterinary Sciences, e University of Queensland, Gatton. In developing this section of the report, Dr Traub used literature searches using PubMed (search terms used = “Parasite Name” + Australia) together with personal communications with experts in academia and the Department of Agriculture, Fisheries and Forestry (DAFF), Queensland Health, and Food Standards Australia.

A8.3.2 Data availability in humans and food attribution Surveillance systems in place include the National Animal Health Information System (NAHIS) and National Noti able Diseases Surveillance System (NNDSS), which collect, collate, analyse and report on data on animal and human health status. In general, information with regard to the incidence or burden of foodborne parasites in humans and animals in Australia is lacking, but is assumed to be negligible. Although limited, most data is generated from research-based surveys conducted by academic institutes, together with published hospital case reports. Surveillance (end product testing for foodborne parasites) is usually not considered necessary due to the low perceived risks to public health, based on: • High standards of food safety and inspection practices that utilize a ‘wholeof-chain’ approach, which includes implementation of risk-based hazard analysis and HACCP. In addition to this, all exported food must comply with the Export Control (Prescribed Goods - General) Orders 2005, and the Export Control (Plants and Plant Products) Orders, 2005. Exporters must meet both the requirements of relevant export legislation and of any importing country requirements for the Australian Quarantine and Inspection Service (AQIS) to provide the necessary documentation to enable products to be exported. • The dietary habits of most Australians, namely eating medium- to wellcooked meats. • The absence of many of the food borne parasites of public health concern in Australia (exotic pathogens). Except for Cryptosporidium, no other foodborne parasites are listed in the human noti able diseases list. For example, cystic hydatid disease in humans is no longer noti able on a state or national level, despite its enzootic nature in rural settings. Many of the sh- and plant-borne parasites (e.g. Anisakiasis, plant- or vector-borne protozoa and helminth infections) may be missed unless an ‘obvious outbreak’ has been detected and reported to the State Public Health Unit. Primary

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means of surveillance of foodborne parasites are performed through abattoirs due to export certi cation requirements, such as data on the incidence of suspect Cysticercus bovis lesions in beef and Trichinella in game meat, and exports would be well documented.

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219

220 Global level Disease in humans? Disease severity and main populations at risk Main food sources and attributions Disease severity and Main food source and main population(s) attribution at risk Yes [22] Yes Yes – anecdotal from case history [21] Yes [13] Yellow eye mullet, tiger athead, sea mullet, King George whiting, bream, sand athead, pilchard Yes. Most outbreaks water-borne recreational swimming. Other sporadic outbreaks ‘Unknown’ source [22] Yes – quantitative data on prevalence in wild and farm dogs [20] No attribution to food. No data No data Yes Indigenous Australians [23] Immuno-suppressed HIV/AIDs patients [24] Yes Indigenous Australians [23] No data No data Wild boar, snake Beef – 100% meat-borne [11] Cattle – 100% foodborne

TABLE A8.3.1 Data availability on the burden of disease and food attribution at the regional and global level for Australia

Data availability on human-disease-related parameters Regional level

Parasite species

Disease in humans?

Angiostrongylus cantonensis Yes – qualitative – Yes – qualitative – case reports [21] case reports [21] [12] Anisakis spp.; Contracaecum Yes No data spp.

Cryptosporidium spp. (including C. hominis and C. parvum)

Yes [22]

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Echinococcus granulosus

Enteric protozoa Giardia, Cyclospora, Blastocystis, Dientamoeba fragilis, Isospora belli

Yes – retrospective hospital cases. Not noti able since 2000 [19] No data

Enteric helminths; Ascaris; Trichuris; hookworms

No data

Spirometra or sparganosis Taenia saginata

No data No data

Data availability on human-disease-related parameters Regional level Global level Disease in humans? Disease severity and main populations at risk Main food sources and attributions Disease severity and Main food source and main population(s) attribution at risk Yes – quantitative serological data [17] Kangaroo meat; lamb (sheep); pigs [16, 18]

Parasite species

Disease in humans?

Toxoplasma gondii

Trichinella papuae in Torres Strait Islands

No data 0.6% posterior uveitis – Aboriginal Australians [14] 3.5% of encephalitis hospitalizations; down since 1990s (HIV peak) [15] 2 reported outbreaks (raw lamb and kangaroo) [16] Yes – qualitative No data anecdotal reports[1, 2] Wild boar (Sus scrofa) [3] Imported crocodile meat from PNG 4] Yes [5, 6] Yes [5, 7]

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Trichinella pseudospiralis – Tasmania

No data

Dasyurids (quolls; Tasmanian devil,) and carrion-feeding birds (marsh harrier, masked owl) [9] Purely sylvatic cycle

Yes [6, 10]

Yes [7, 10]

Domestic and wild boar [5] Crocodile meat, turtle meat [8] 100% foodborne Domestic and wild boar [9] 100% foodborne

221

Sources used in Table A8.3.1

01.

02. 03.

04. 05.

06. 07. 08.

09.

10. 11.

12. 13.

14.

15.

16.

Spratt, D.M., Beveridge, I., Andrews, J.R.H. & Dennett, X. 1999. Haycocknema perplexum n.g., n.sp. (Nematoda: Robertdollfusidae): an intramyo bre parasite in man. Systematic Parasitology, 43(2): 123–131. Department of Primary Industries (DPI) report. No date. Three human clinical cases in Adelaide (archived, pers. comm. Jack van Wick). Cuttell, L., Cookson, B., Jackson, L.A., Gray, C. & Traub, R.J. 2012. First report of a Trichinella papuae infection in a wild pig (Sus scrofa) from an Australian island in the Torres Strait region. Veterinary Parasitology, 185(2-4): 343–345. Louise Jackson, DAFF, pers. comm. Kusolsuk, T., Kamonrattanakun, S., Wesanonthawech, A. and 11 others. 2010. The second outbreak of trichinellosis caused by Trichinella papuae in Thailand. Transactions of the Royal Society of Tropical Medicine and Hygiene, 104(6): 433– 437. WHO. Various dates (a). Total cases and incidence of Trichinella spp. infections, by World Health Organization region and country, 1986–2009. WHO. Various dates (b). Clinically con rmed cases of trichinellosis in humans documented in World Health Organization regions, 1986–2009. Lo, Y.-C., Hung, C.-C., Lai, C.-S., Wu, Z., Nagano, I., Maeda, T., Takahashi, Y., Chiu, C.H. & Jiang, D.D.-S. 2009. Human trichinosis a er consumption of so -shelled turtles, Taiwan. Emerging Infectious Diseases, 15(12): 2056–2058. Obendorf, D.L. & Clarke, K.P. 1992. Trichinella pseudospiralis infections in free-living Tasmanian birds. Journal of the Helminthological Society of Washington, 59(1): 144– 147; Obendorf, D.L., Handlinger, J.H., Mason, R.W., Clarke, K.P., Forman, A.J., Hooper, P.T., Smith, S.J. & Holdsworth, M. 1990. Trichinella pseudospiralis infection in Tasmanian wildlife. Australian Veterinary Journal, 67(3): 108–110. Murrell, K.D. & Pozio, E. 2011. Worldwide occurrence and impact of human trichinellosis 1986–2009. Emerging Infectious Diseases, 17(12): 2194–2202. Jenkins et al., under review. Cysticercosis in beef cattle in New South Wales. Submitted to Australian Veterinary Journal. Under review; Pearse, B.H.G., Traub, R.J., Davis, A., Cobbold, R. & Vanderlinde, P.B. 2010. Prevalence of Cysticercus bovis in Australian cattle. Australian Veterinary Journal, 88(7): 260–262; Brown, G., Dennis, M.M., Slapeta, J. & Thompson, A.R. 2010. Prevalence of Cysticercus bovis (beef measles) in Australian cattle. [Comment on Pearse et al., 2010, q.v... Australian Veterinary Journal, 88(12): 463–464. Shamsi, S. & Butcher, A.R. 2011. First report of human anisakidosis in Australia. Medical Journal of Australia, 194(4): 199–200. Shamsi, S., Eisenbarth, A., Saptarshi, S., Beveridge, I., Gasser, R.B. & Lopata, A.L. 2011. Occurrence and abundance of anisakid nematode larvae in ve species of sh from southern Australian waters. Parasitology Research, 108(4): 927–934; Lymbery, A.J., Doupe, R.G., Munshi, M.A. & Wong, T. 2002. Larvae of Contracaecum sp. among inshore sh species of south-western Australia. Diseases of Aquatic Organisms, 51(2): 157–159. Chang, J.H., Landers, J., Henderson, T.R.M. & Craig, J.E. 2012. Prevalence of uveitis in indigenous populations presenting to remote clinics of central Australia: The Central Australian Ocular Health Study. Clinical And Experimental Ophthalmology, 40(5): 448–453. Huppatz, C., Durrheim, D.N., Levi, C., Dalton, C., Williams, D., Clements, M.S. & Kelly, P.M. 2009. Etiology of encephalitis in Australia, 1990–2007. Emerging Infectious Diseases, 15(9): 1359–1365. Parameswaran, N., O’Handley, R.M., Grigg, M.E., Fenwick, S.G. & Thompson, R.C.A. 2009. Seroprevalence of Toxoplasma gondii in wild kangaroos using an ELISA. Parasitology International, 58(2): 161–165.

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MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

17.

18. 19. 20.

21.

22. 23.

24.

25.

Plant, J.W., Freeman, P. & Saunders, E. 1982. Serological survey of the prevalence of Toxoplasma gondii antibodies in rams in sheep ocks in New South Wales. Australian Veterinary Journal, 59(3): 87–89. Munday, B.L. 1975. Prevalence of toxoplasmosis in Tasmanian meat animals. Australian Veterinary Journal, 51(6): 315–316. Jenkins, D.J. & Power, K. 1996 Human hydatidosis in New South Wales and the Australian Capital Territory, 1987–1992. Medical Journal of Australia, 164(1): 18–21. Jenkins, D.J., Allen, L. & Goullet, M. 2008. Encroachment of Echinococcus granulosus into urban areas in eastern Queensland, Australia. Australian Veterinary Journal, 86(8): 294–300; Jenkins, D.J., McKinlay, A., He, D.L., Bradshaw, H. & Craig, P.S. 2006. Detection of Echinococcus granulosus coproantigens in faeces from naturally infected rural domestic dogs in south-eastern Australia. Australian Veterinary Journal, 84(1-2): 12–16. Prociv, P. & Carlisle, M.S. 2001. The spread of Angiostrongylus cantonensis in Australia. Southeast Asian Journal of Tropical Medical Public Health, 32(Suppl. 2): 126–128. OzFoodNet. Various dates. Communicable Diseases Australia quarterly reports. Holt, D.C., McCarthy, J.S. & Carapetis, J.R. 2010. Parasitic diseases of remote indigenous communities in Australia. International Journal for Parasitology, 40(10; Special issue): 1119–1126. Stark, D., Barratt, J.L.N., van Hal, S., Marriott, D., Harkness, J., & Ellis, J.T. 2009. Clinical signi cance of enteric protozoa in immunosuppressed human populations. Clinical Microbiology Reviews, 22(4): 634–640. B. Cookson, Biosecurity O cer, Northern Australian Quarantine Strategy, Department of Agriculture, Fisheries & Forestry, Australian Government. Pers. comm., 2011.

TABLE A8.3.2 Data availability for Australia for parasite prevalence or concentration in the main food categories Angiostrongylus cantonensis Other No direct data. Some snail surveys. Anecdotal evidence of increase in incidence in domestic pets and wildlife in urban areas of Brisbane and Sydney. Human case reported from ingesting slugs while intoxicated [1]

Anisakis spp., Contracaecum spp. Seafood Little data. Prevalence in Yellow eye mullet, athead, sea mullet, King George Whiting, Bream, sand athead, pilchard described and endemic o coastal Australia. Most larvae in viscera post-harvest and not muscle [2, 3]. Yes. Wild caught and commercial sh at post-harvest level.

Other

Cryptosporidium spp. (including C. hominis and C. parvum) Beef Dairy Pork Game Seafood Yes Yes No data No data Yes [4]. Reported Cryptosporidium oocyst contamination of some high-risk foods.

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Fruits Vegetables Other

Yes [4]. Reported Cryptosporidium oocyst contamination of some high-risk foods. Yes [4]. Reported Cryptosporidium oocyst contamination of some high-risk foods. Goat meat (India)

Echinococcus granulosus Vegetables Other No data No direct data. Abattoir reports suggest hydatid disease is still highly endemic among livestock. Prevalence studies in dogs, esp. in rural areas, also demonstrate high prevalence among farm dogs [5, 6]

Enteric helminths: Ascaris, Trichuris, Hookworms Fruits Vegetables No data No data

Enteric protozoa: Giardia, Cyclospora, Blastocystis, Dientamoeba fragilis, Isospora belli Fruits Vegetables No data No data

Spirometra erinacei or sparganosis Quantitative data may be obtained from Biosecurity Queensland records. Endemic in tropics, esp. wild boar, native frogs, feral cats, dogs. Pork Game Other No data No data Wild boar Northern Australian Quarantine Strategy (NAQS) surveys

Taenia saginata or bovine cysticercosis Beef Incidence estimated to be less than 1 in 500 000 head according to a recent national survey [7]. However sporadic cases or outbreaks, although rare, are known to occur and have subsequently been con rmed as C. bovis [8, 9].

Toxoplasma gondii Beef Dairy Pork Poultry Game Fruits Vegetables Other Yes [10]. Most cited references in report from 1975 and 1980s. Yes [10]. Most cited references in report from 1975 and 1980s. Yes [10]. Most cited references in report from 1975 and 1980s. Yes [10]. Most cited references in report from 1975 and 1980s. Yes [10]. Most cited references in report from 1975 and 1980s. No data No data Pademelons, wallabies, lamb. 15.5% kangaroos from WA positive by ELISA [11].

Trichinella papuae, T. pseudospiralis Pork No data

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Poultry Game

No data Yes. All horse, crocodile and wild pig exported to EU from mainland Australia undergoes pooled Arti cial Digestion technique (AD). To date no larvae detected on mainland. Recent research-based survey using AD and polymerase chain reaction (PCR) detected 2 pigs positive for larvae/DNA of T. papuae on a remote island of the Torres Strait [15]. Moreover, recent serological evidence for Trichinella on mainland [12, 14]. Foxes and wild dogs on mainland. Tasmanian quolls, possums, raptoral birds [19, 20]. Limited indicator species testing on mainland (200 rats; 60 foxes, 31 wild dogs, 9 cats, 27 quolls) tested by AD, all negative [16–18].

Other [14]

Sources used for Table A8.3.2

01. 02.

03.

04. 05.

06.

07.

08.

09.

10.

11.

Richard Mailk & McCarthy, pers. comm., 2012. Shamsi, S., Eisenbarth, A., Saptarshi, S., Beveridge, I., Gasser, R.B. & Lopata, A.L. 2011. Occurrence and abundance of anisakid nematode larvae in ve species of sh from southern Australian waters. Parasitology Research, 108(4): 927–934; Lymbery, A.J., Doupe, R.G., Munshi, M.A. & Wong, T. 2002. Larvae of Contracaecum sp. among inshore sh species of south-western Australia. Diseases of Aquatic Organisms, 51(2): 157–159. Smith, H.V. & Nichols, R.A.B. 2010. Cryptosporidium: Detection in water and food. Experimental Parasitology, 124(1; Special Issue): 61–79. Jenkins, D.J., McKinlay, A., He, D.L., Bradshaw, H. & Craig, P.S. 2006. Detection of Echinococcus granulosus coproantigens in faeces from naturally infected rural domestic dogs in south eastern Australia. Australian Veterinary Journal, 84(12): 12–16. Jenkins, D.J., Allen, L. & Goullet, M. 2008. Encroachment of Echinococcus granulosus into urban areas in eastern Queensland, Australia. Australian Veterinary Journal, 86(8): 294–300. Pearse, B.H.G., Traub, R.J., Davis, A., Cobbold, R. & Vanderlinde, P.B. 2010. Prevalence of Cysticercus bovis in Australian cattle. Australian Veterinary Journal, 88(7): 260–262; Brown, G., Dennis, M.M., Slapeta, J. & Thompson, A.R. 2010. Prevalence of Cysticercus bovis (beef measles) in Australian cattle. [Comment on Pearse et al., 2010, q.v.]. Australian Veterinary Journal, 88(12): 463–464. Jenkins, D.J., Brown, G.K. & Traub, R.J. 2012. Cysticercosis “storm” in cattle in feedlot cattle in north-west New South Wales. Australian Veterinary Journal 91(3): 89–93. Lake, R., Hudson, A. & Cressey, P. 2002. Risk pro le: Toxoplasma gondii in red meat and meat products. Prepared as part of a New Zealand Food Safety Authority contract for scienti c services. 36 p. See: http:/ /www.foodsafety.govt.nz/elibrary/ industry/Risk_Pro le_Toxoplasma-Science_Research.pdf Parameswaran, N., O’Handley, R.M., Grigg, M.E., Fenwick, S.G. & Thompson, R.C.A. 2009. Seroprevalence of Toxoplasma gondii in wild kangaroos using an ELISA. Parasitology International, 58(2): 161–165.

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12.

14.

15.

16. 17. 18.

19.

20.

Cuttell, L., Gomez-Morales, M.A., Cookson, B., Adams, P.J., Reid, S., Vanderlinde, P., Jackson, L.A. & Traub, R.J. [2013]. Evaluation of ELISA coupled with con rmatory testing as a surveillance tool for Trichinella infection in wild boar. In preparation. Cuttell, L., Corley, S.W., Gray, C.P., Vanderlinde, P.B., Jackson, L.A. & Traub, R.J. 2012. Real-time PCR as a surveillance tool for the detection of Trichinella infection in muscle samples from wildlife. Veterinary Parasitology, 188(3-4): 285–293. Cuttell, L., Cookson, B., Jackson, L.A., Gray, C. & Traub, R.J. 2012. First report of a Trichinella papuae infection in a wild pig (Sus scrofa) from an Australian island in the Torres Strait region. Veterinary Parasitology, 185(2-4): 343–345. Jenkins, D.J. & Pozio, E. unpublished data, cited in Pozio, E. & Murrell, K.D. 2006. Systematics and epidemiology of Trichinella. Advances in Parasitology, 63: 367–439. Waddell, A.H. 1969. The search for Trichinella spiralis in Australia. Australian Veterinary Journal, 45(4): 207. Oakwood, M. & Spratt, D.M. 2000, Parasites of the northern quoll, Dasyurus hallucatus (Marsupialia: Dasyuridae) in tropical savanna, Northern Territory. Australian Journal of Zoology, 48: 79–90. Obendorf, D.L. & Clarke, K.P. 1992. Trichinella pseudospiralis infections in freeliving Tasmanian birds. Journal of the Helminthological Society of Washington, 59(1): 144–147. Obendorf, D.L., Handlinger, J.H., Mason, R.W., Clarke, K.P., Forman, A.J., Hooper, P.T., Smith, S.J. & Holdsworth, M. 1990. Trichinella pseudospiralis infection in Tasmanian wildlife. Australian Veterinary Journal, 67(3): 108–110.

A8.3.3 Agri-food trade Foodborne parasites that currently have implications for the meat industry in terms of extra costs associated with inspection and testing are primarily restricted to C. bovis in the domestic and exported beef industry, and Trichinella testing of game meat (farmed crocodile, wild boar and horses) destined for the EU. However, for example, were anisakidosis to become an emerging public health problem in Australia, the sh industry would have to bear the costs of additional end-product inspection (e.g. candling, pooled PCR) to certify high-risk marine species safe for consumption. Bovine cysticercosis Although rare, sporadic cases of C. bovis continue to be reported in the beef industry. Carcasses heavily positive for suspect C. bovis lesions are condemned, whereas those with low levels of infection are excluded from the export chain. Any visible lesions are trimmed at boning under veterinary supervision, freeze certi ed and sold on the domestic market. At present the abattoirs (industry) bear the cost of positively inspected carcasses. ere is a move to reform this and place more cost and responsibility on the farmer by bringing in on-plant monitoring schemes that feed back to the farm level, providing incentive for modi cation or improvements in farm management. Given the low incidence of bovine cysticercosis and poor positive predictive value of organoleptic inspection, a risk-based system for inspecting C. bovis is being proposed and reviewed (Webber et al., 2012).

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Trichinella spp. At present, game meat (wild boar, horse, crocodile) destined for the EU (primary consumers) is required to undergo pooled arti cial digestion and examination for Trichinella larvae, and results in a direct cost to the game meat industry. To date, testing of ~3.2 million wild boars and 300 000 horses over 22 years has yielded no Trichinella-positive carcasses. However, wildlife surveys in indicator species (foxes, feral cats, crocodiles, turtles and wild boar in high-risk areas, e.g. northern Queensland, are limited. Detection of Trichinella on mainland Australia will most likely have most impact on the domestic pork industry in relation to more intensive pre-harvest control measures required to meet domestic and overseas certi cation of pig farms as Trichinella-free. At present, domestic pork exported is freeze-certi ed for Trichinella.

A8.3.4 Consumer perception Consumer perception is di cult to assess and is largely dependent on approaches taken by the media and government in the form of risk communication to the public in the case of an ‘outbreak’ or discovery of a previously ‘exotic’ or ‘undetected’ foodborne parasite. At present, Australians are generally aware of governmental responsible for regulating the quality and safety of food, and consumers display considerable trust in government (and farmers) to protect food safety. ere is little evidence of the politicization of food, re ecting a level of trust in the Australian food governance system that may arise from a lack of exposure to major food scares. Consumers tend to be more critical of the role of the food industry in food safety, believing that pro t motives will undermine e ective food regulation. Most Australians would associate foodborne illness with ‘take-away’ foods from retail outlets or a problem associated with overseas travel. Consumers usually perceive the risk of ‘parasites’ in game meats like kangaroos and feral pigs higher than traditional meats. Australians are generally aware of personal responsibility for food safety practices (Henderson, Coveney and Ward, 2010). Consumers (public) in overseas markets are likely to have a similar level of ‘trust’ in foods exported from Australia.

A8.3.5 Social sensitivity If an ‘outbreak’ of a foodborne parasitic disease due to non-compliance with current food safety regulations or due to consumers harvesting their own food sources (in the case of home-grown vegetables, home-made sh sashimi or undercooked foods, hunted feral pig or crocodile meat, etc.) should occur, this has the potential to lead to a substantial decline in the level of consumer trust placed in the food safety management system of Australia. is will have signi cant repercussions on the industry in some cases (e.g. outbreak of anisakiasis may lead to loss of business for Japanese restaurants or sea-food retailers). An outbreak of trichinello-

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sis may have similar consequences, but to a lesser extent as the public is more likely to associate the pathogen with consumption of self-butchered game meat rather than commercially supplied meats.

A8.3.6 Risk management Data are summarized in Table A8.3.3.

A8.3.7 Sources cited in the discussion Henderson, J.A.B., Coveney, J.A. & Ward, P.A. 2010. Who regulates food? Australians’ perceptions of responsibility for food safety. Australian Journal of Primary Health, 16(4): 344–351. Webber, J.J., Dobrenov, B., Lloyd, J. & Jordan, D. 2012. Meat inspection in the Australian red-meat industries: past, present and future. Australian Veterinary Journal, 90(9): 363–369. TABLE A8.3.3 Data availability for risk management options for each of parasite-commodity combinations for Australia. NOTE: The authors were asked to consider all combinations of the particular parasite and the main food categories, namely Beef, Dairy, Pork, Poultry, Game, Seafood, Fruit, Vegetables and Other.

Angiostrongylus cantonensis Fruits No data Vegetables No data Other No – snails Anisakids Seafood Little data. Extensive surveys performed for the Australian marine sh/ anisakid species. No experimental studies to determine post-harvest migration or larvae for Australian species. Preliminary research surveys (see Table A8.3.1) indicate larvae primarily in viscera, current FSANZ food safety Standard 4.2.1 [5] stipulates chilling (-1°C to 5°C or lower) post-harvest. All exported sh frozen to inactivate larvae. Cryptosporidium spp. (including C. hominis and C. parvum) Other The prevalence or intensity of protozoa, helminth and cestode stages contaminating fresh produce along the production chain is not readily available. However, in general, risk is mitigated by producer obligations to follow standards outlined by the Codex Code of Hygienic Practice for Fresh Fruits and Vegetables. Echinococcus granulosus Fruits No data Vegetables No data Enteric helminths No data.

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Enteric protozoa, including Giardia, Cyclospora, Blastocystis, Dientamoeba fragilis and Isospora belli No data. Taenia saginata or bovine cysticercosis Beef Yes [1, 2]. See also Table A8.3.1 Other Low incidence and poor PPV of inspection of predilection sites – more emphasis on farm-level management to reduce risks. Toxoplasma gondii Regionally, a risk pro le [3] was conducted by New Zealand Food Safety Authority, based on outdated prevalence data for retail raw meats. Globally, the requirements for inactivation of tissue cysts in meat have been well studied and documented. Beef Yes qualitative. Quantitative lacking on % positive retail meats with viable tissue cysts lacking. Dairy Food Standards Australia New Zealand (FSANZ) Standard 4.2.4 – Primary Production and Processing Standard for Dairy Products Pork Yes qualitative. Quantitative lacking on % positive retail meats with viable tissue cysts lacking Poultry Yes qualitative. Quantitative lacking on % positive retail meats with viable tissue cysts lacking Game Yes qualitative. Quantitative lacking on % positive retail meats with viable tissue cysts lacking Fruits No data Vegetables No data Trichinella papuae, T. pseudospiralis Pork No data Game No extensive surveys in ‘hot-spots’ Experimental studies in pigs for T. papuae lacking to assess survivability, freeze tolerance Other No surveys on the mainland. A small-scale survey in feral pigs by Cuttell [4] (see Table A8.3.1) allowed a qualitative risk assessment to be attempted. Sources cited in Table A8.3.3 01. 02. Pearse, B.H.G., Traub, R.J., Davis, A., Cobbold, R. & Vanderlinde, P.B. 2010. Prevalence of Cysticercus bovis in Australian cattle. Australian Veterinary Journal, 88(7): 260–262; Webber, J.J., Dobrenov, B., Lloyd, J. & Jordan, D. 2012. Meat inspection in the Australian red-meat industries: past, present and future. Australian Veterinary Journal, 90(9): 363– 369. Lake, R., Hudson, A. & Cressey, P. 2002. Risk pro le: Toxoplasma gondii in red meat and meat products. Prepared as part of a New Zealand Food Safety Authority contract for scienti c services. 36 p. See: http:/ /www.foodsafety.govt.nz/elibrary/industry/Risk_ Pro le_Toxoplasma-Science_Research.pdf Cuttell, L., Cookson, B., Jackson, L.A., Gray, C. & Traub, R.J. 2012. First report of a Trichinella papuae infection in a wild pig (Sus scrofa) from an Australian island in the Torres Strait region. Veterinary Parasitology, 185(2-4): 343–345. FSANZ (Food Safety Australia New Zealand). 2012. Australia New Zealand Food Standards Code - Standard 4.2.1 - Primary Production and Processing Standard for Seafood (Australia Only). Current. See: http:/ /www.comlaw.gov.au/Series/F2012L00291

03.

04.

05.

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229

ANNEX 8.4 EUROPE A8.4.1 Preparation e information was compiled by a group comprising Lucy Robertson, Norway (Group leader-cum-coordinator); Pascal Boireau, France; Joke van der Giessen, e Netherlands; Malcolm Kennedy, Scotland, UK; and Patrizia Rossi, Italy, although Patrizia was away during report writing, and thus contributed only information. Communication among the group members was largely by e-mail, and the nal version (following inclusion of comments on and modi cations to the dra ) was submitted on 20 August. e di erent group members used their own approaches to data gathering, accessing: • published scientific papers (identified using their knowledge and experience of the topic, coupled with appropriate database searches; • national reports or risk assessments, or both; • the European Union Reference Laboratory for Parasites (EURLP) in Rome (http://www.iss.it/crlp/), • scientific reports submitted to European Food Safety Authority (EFSA); • reports from World Organisation for Animal Health (OIE), World Health Organization (WHO), and European Centre for Disease Prevention and Control (ECDC); • reports from EU research groups (e.g. MedVetNet, Echinorisk); • Codex Alimentarius Commission reports; and • books and book chapters.

A8.4.2 Data availability in humans and food attribution Data from Europe is patchy. EFSA has had initiatives in which data concerned with meat-borne parasites (Sarcocystis spp., Toxoplasma spp., Trichinella spp., Taenia solium and Taenia saginata), Echinococcus spp. and sh-borne parasites (particularly Anisakis simplex) have been reported, including proposals for harmonized monitoring tools. ese reports give a relatively good overview of the data available in EU member states. Although Sarcocystis spp. is probably widespread, the low public and zoonotic health impact means that Sarcocystis spp. should not be considered a parasite of major concern in Europe.

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Data on distribution regarding Taenia spp. is patchy, but taeniosis and/or cysticercosis caused by T. solium in humans in Europe is considered rare. Data on Toxoplasma gondii and Trichinella spp. is relatively good, particularly for the latter parasite and for Toxoplasma spp. if mandatory screening is in place; both, particularly T. gondii in high risk groups, are considered of importance. Data on Echinococcus (E. granulosus sensu lato and E. multilocularis) are patchy; this is largely due to lack of noti cations, diagnostic di culties and uneven distribution of infection around Europe, although evidence suggests that E. multilocularis infection is spreading in foxes in Europe, resulting in greater infection risk in humans. Data on infection with intestinal protozoa such as Cryptosporidium, Giardia and Cyclospora are patchy, being, relatively good in some places (e.g. United Kingdom), but poor in others, but whether sporadic infections are foodborne or not is usually impossible to ascertain; some outbreaks have been shown to be foodborne. Data on infection with trematodes and nematodes is patchy unless associated with speci c outbreaks. It can be assumed that many foodborne parasitic infections in Europe are not diagnosed, due to non-speci c symptoms, or, if they are diagnosed, foodborne transmission is not recognized, particularly for sporadic cases not associated with outbreaks.

A8.4. 3 Data on the burden of disease and food attribution See Table A8.4.1.

A8.4.4 Data on parasite prevalence, incidence and concentration in the main food categories e data are summarized in Table A8.4.2.

A8.4.5 Agri-food trade Agri-food trade is a ected when parasite contamination is found in imported products, particularly if: a) the imported parasite does not exist in the region previously and/or b) an outbreak of infection results. Meat Meat on the market must be free of Trichinella larvae, and metacestodes of Taenia and Echinococcus. Some countries also regulate against Sarcocystis, such as the

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231

Italian requirement from 1992 for restaurants to freeze shes to be served raw or undercooked. Meat inspection is used for metacestodes (and sarcocysts). For Trichinella, a speci c lab analysis (digestion) is used. For the EU there are de nitive regulations (EU legislation on the hygiene of foodstu s). ere is a meat inspection on target hosts. Only Trichinella needs a speci c laboratory analysis. e cost and reliability of this analysis is important to take into account in the balance of cost vs bene t. Some one-third of European countries impose individual carcass control for Trichinella as a requirement for exportation. Trichinella “negligible risk” areas were de ned in Europe to reduce the cost of individual carcass control. However, for trade in pig meat, countries ask for individual carcass control even from negligible risk areas. Currently, harmonized risk-based control strategies are evaluated by OIE, Codex and EU bodies. Exotic meats are also subject to these controls (e.g. crocodile meat and T. zimbabwensis). Although Toxoplasma is a high risk in meat, it is so widespread that it does not a ect the agri-food business at present. Currently, no speci c regulations are in place to identify Toxoplasma in meat. Seafood ere has been a signi cant increase in sh or seafoodborne parasitic diseases in Europe, caused either by infection following ingestion of viable parasites or as an allergenic reaction against parasite antigens (hypersensitivity). Due to modern cooking habits, there is a need to harmonize control measures for sh to decrease the risk of sh-borne parasites. In the EU, raw sh meant for human consumption (herring, salmon) should be frozen before consumption, but more and more raw or undercooked sh (which is unregulated for parasites) is being consumed nowadays. In Europe, the most important sh parasites causing illness in humans are from the Anisakidae family, with 24 genera, although the species most commonly associated with human infection is Anisakis simplex, followed by Pseudoterranova decipiens. Nevertheless A. simplex is the primary instigator of the di erent forms of allergy, triggered by infection by live larvae. However, it is not known if this increase in parasitic disease has a ected agri-food trade. Human outbreaks of Opisthorchis infection have been identi ed (e.g. Italy, the Netherlands), but it is not clear whether this has a ected agri-food trade. Fresh produce Outbreaks associated with contaminated fresh produce may a ect agri-food trade (as exempli ed by the raspberries/Cyclospora impact on import to North America from Guatemala). Although there have been outbreaks of parasitic infection as-

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sociated with imported fresh produce in Europe (e.g. in Sweden, Cyclospora on sugarsnap peas from Guatemala; Cryptosporidium on parsley from Italy), there do not appear to have been long-term e ects on agri-food trade. Similarly, it is unclear whether outbreaks associated with local fresh-produce (e.g. Fasciola on watercress in France) have a ected agri-food trade exports. Conclusion Important parasite-commodity combinations that could a ect agri-food trade in Europe include: meat+Trichinella; meat+Taenia; meat+Echincoccus; sh+all parasites, including ukes; fresh produce+Cryptosporidium; fresh produce+Cyclospora; fresh produce+Giardia; and fresh produce+Fasciola. Current concern seems to be more for public health and food import than for trade and export. However, this situation is likely to change should an extensive outbreak be associated with an exported European food product.

A8.4.6 Consumer perception ere have been no speci c surveys at EU level to analyse consumer perceptions regarding the risks generated by parasites in food, although there have been various general surveys performed in Europe or speci c countries. One of the most relevant is from 2005 (Anon. 2006), in which the then 25 countries of the EU (without Romania and Bulgaria, which joined the EU in 2007) were interviewed to assess consumer risk perceptions, particularly regarding food safety. Although foodborne parasitic infections were not speci cally addressed, the survey demonstrated that the major concerns regarding food safety in the EU were directed towards pesticide residues in fruit, vegetables and cereals; residues such as antibiotics and hormones in meats; unhygienic conditions in food processing plants, shops or restaurants’ contamination with bacteria (food poisoning); pollutants such as mercury or dioxins; genetically modi ed products; and additives such as colours, preservatives or avourings. According to the survey results, on a country basis, the Greeks, Italians and Cypriots were the biggest worriers about food contamination issues, but respondents in Sweden and Finland worried the least. Nordic countries also appeared to have greater con dence in public authorities concerning provision of information on speci c food safety issues, with Finland demonstrating the greatest con dence in the authorities. Globally, consumers tend to have more trust in vegetables and fruits than meat products when it comes to safety (Anon., 2004). Fewer respondents thought that food was become worse with regard to safety. A locally or regionally adapted food-risk communication is preferred by EU consumers, and may be more e cient that a pan-European communication, due to di erent culinary habits across Europe and di ering parasite densities transmitted in di erent regions.

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However, harmonized communication on the risks for foodborne parasites, e.g. Echinococcus multilocularis, is needed, as risk communication is currently scattered and inconsistent. Outbreaks obviously a ect consumer perceptions considerably (perhaps out of proportion to the risk), and this again means that communication is important.

A8.4.7 Social sensitivity e presence of Anisakis in sh meat is not acceptable. Even if the meat is frozen there is a risk of allergenicity. is secondary danger is not well known by consumers. In addition, the nding of parasites in sh food during consumption (visual) engenders emotional reactions, and even if the public health risk is low, it is unacceptable to European consumers. Consumers expect meat to be parasite-free. For parasites in meat that are not visible to the naked eye (Sarcocystis, Toxoplasma), restrictions are important if local culinary habits (raw or undercooked meat consumption) increase infection risk. e detection and reporting of a parasite risk in meat (or probably any other food commodity) induces an immediate drop in consumption. is was particularly well studied during trichinellosis in France (1986–1998) a er infection of consumers eating horse meat. e increased risk of parasitic infections when organic meat is consumed is not well understood by the public. In general, people believe that organic products are more healthy, which is usually not the case regarding parasitic risks. Some ‘organic products’ may, however, be perfectly acceptable produce, but it should also be recognized that specialist producers are most likely to be a ected should an outbreak reported in the media be speci cally associated with their specialization, regardless of their own standards, epitomized by the recent furore over alfalfa sprouts and bacterial infection. Food sovereignty is an important concept regarding developing countries exporting produce (meat, sh, fresh produce) to wealthier countries that may ultimately reject on microbiological grounds or for other reasons. is concept is being explored in some research projects (e.g. Veg-i-Trade, see: www.vegitrade.com). e parasite-commodity combinations that are probably most relevant from a European perspective are: meat+Trichinella; meat+Taenia; meat+Echincoccus; sh+all parasites, including ukes; fresh produce+Cryptosporidium; fresh produce+Cyclospora; and fresh produce+Giardia. Concern is more for public health and food imports than for trade and exports.

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A8.4.8 Risk management e data are summarized in Table A8.4.3.

A8.4.9 Sources cited in the text of the Europe section discussion

Anon[ymous]. 2004. Consumer Trust in Food. A European Study of the Social and Institutional Conditions for the Production of Trust. e TRUSTINFOOD project (2002-2004) is supported by the European Commission, Quality of Life and Management of Living Resources Programme (QoL), Key Action 1 Food, Nutrition and Health (contract no. QLK1-CT-2001-00291). For further information sSee: http:// www.academia.edu/307738/Trust_and_Food._A_ eoretical_Discussion Anon. 2006. Risk Issues. Special Eurobarometer 238 / Wave 64.1. prepared by TNS Opinion & Social for Directorate-General Health and Consumer Protection as well as the European Food Safety Authority and coordinated by DirectorateGeneral. See: http://ec.europa.eu/food/food/resources/special-eurobarometer_ riskissues20060206_en.pdf

CHAPTER 1 INTRODUCTION

235

236 Global level Main food source and attribution no no Disease in humans Disease severity/ main populations at risk Man food sources and attributions Disease severity/ main populations at risk no Yes [32, 33] No data Hypersensitivity risk and infection risk Yes [32, 33] Infection risk: uncooked, lightly salted/smoked/ pickled sh Hypersensitivity risk: as above, but also cooked or frozen sh Yes Fresh produce – fruit, vegetables Yes Yes [26, 27] Consumption of wild boar meat contaminated with larvae. Consumption of frog is questionable. Yes [32, 33] Yes [32, 33] Hypersensitivity risk Infection risk: and infection risk uncooked, lightly salted/smoked/pickled sh Hypersensitivity risk: as above, but also cooked or frozen sh Yes Yes Toxocara infection Fresh produce – fruit, may result in vegetables ocular problems; association with allergy Yes [32, 38–42] Yes [32, 38–42] ImmunoWater and food compromised, (fresh produce, milk) young contaminated by oocysts Yes [42] Yes May result in ocular problems. May exacerbate other problems such as malnutrition Yes [42] Immunocompromised, young Yes [42] Water and food (fresh produce, milk, apple juice, raw meat) contaminated by oocysts

TABLE A8.4.1 Data availability on the burden of disease and food attribution at the regional (European) and global levels

Data availability on human disease related parameters

Regional level

Parasite species

Disease in humans

Alaria alata

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Anisakis spp. (and other anisakids)

Yes -very rare. Humans can be paratenic hosts. Yes [32, 33]

Ascaris lumbricoides, Yes Toxocara spp. and other STH

Cryptosporidium parvum, Cryptosporidium hominis & other Cryptosporidium spp. Note A.

Yes [32, 38–42]

Data availability on human disease related parameters Global level Main food source and attribution Yes [47] Yes [47] Disease in humans Disease severity/ main populations at risk Man food sources and attributions

Regional level Disease severity/ main populations at risk Yes [47]

Parasite species

Disease in humans

Cyclospora cayetanensis Yes [36, 37]

Yes [47]

Yes [34–37]

Yes [47] Fresh produce (salad, raspberries) Yes [36, 37] Undercooked freshwater sh Food contaminated by eggs excreted by infected dogs (note that control can aim at meat in the transmission cycle – not feeding viscera to dogs – reducing prevalence in intermediate hosts)

Diphyllobothrium latum and other Diphyllobothrium spp. Echinococcus granulosus Yes

Yes [17, 25]

Yes [36, 37] No data (vitamin B12 de ciency anaemia possible) Yes

Echinococcus multilocularis

Yes [17–23]

Yes [47] Fresh produce (salad, mange tout) Yes [34–37] Yes [34–37] No data (vitamin B12 Undercooked de ciency anaemia freshwater sh possible) Yes [17, 25] Yes [17, 25] Food contaminated by eggs excreted by infected dogs (note that control can aim at meat in the transmission cycle – not feeding viscera to dogs – reducing prevalence in intermediate hosts) Yes [17, 19–22] Yes [17, 19–22] Food (particularly berries) contaminated by eggs excreted by infected canids (dogs, foxes and raccoon dogs) Yes [19] Yes [19] Yes Yes

ANNEX 8 REGIONAL REPORTS

Echinoccocus (non-European species)

No data

Yes [19] Food (particularly berries growing at ground level) contaminated by eggs excreted by infected canids (dogs, foxes and raccoon dogs) Yes [17] Food contaminated by eggs excreted by carnivorous

237

238 Global level Main food source and attribution Yes Watercress Yes [53, 54] Yes [43, 45, 46] Water, fresh produce Yes [46] Yes [46] Yes [53, 54] Yes [53, 54] Lettuce, watercress Yes [46] Water, fresh produce Disease in humans Disease severity/ main populations at risk Man food sources and attributions Disease severity/ main populations at risk Yes People eating watercress Yes [44–46] Rate of 5.6 per 100 000 in 2009. Age group 0–4 years No data No data Yes [29] Yes [30, 31] Yes [30, 31] Yes [29] Depends on species Yes [8] Bovine meat Yes [28] Yes [8] Taeniosis not severe but considered unacceptable. Yes [8] neurocysticercosis Yes [28] Yes [29] Pork or beef, depending on species Yes [7] Yes [7] Yes [8] Taeniosis not severe Bovine meat but considered unacceptable. Yes [7] Yes [7] Yes [8, 9] Taeniosis not severe Pork (adult T. solium but considered infection) unacceptable. Contaminated Cysticercosis is vegetables, etc. severe. (cysticercosis) Yes [11, 13–15] Yes [11–13–15] Yes [16] Pregnant Meat (esp. lamb), women, immunovegetables compromised) contaminated with oocysts (food hygiene) Yes [16] Pregnant women, immunocompromised) Yes [8] Pork (adult T. solium infection) Contaminated vegetables, etc. (cysticercosis) Yes [16] Meat from domestic animal and wild mammals (pork, mutton, venison); milk; food contaminated by oocysts

Data availability on human disease related parameters

Regional level

Parasite species

Disease in humans

Fasciola hepatica and other Fasciola spp. Giardia duodenalis

Yes

Yes [45, 46]

Linguatula serrata

No data

Sarcocystis spp.

Yes [28]

Taenia saginata Yes [7] (syn. Taeniarhynchus saginata)

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Taenia solium

Yes [7, 10] (E. Europe only?)

Toxoplasma gondii

Yes [11, 13–15]

Data availability on human disease related parameters Global level Main food source and attribution Yes [1, 3] 100% foodborne transmission. Meat (infected muscles from mammals (rarely birds)) Yes [1, 2, 4, 5] Yes [1, 2, 4, 5] Yes Yes Yes Disease in humans Disease severity/ main populations at risk Man food sources and attributions

Regional level Disease severity/ main populations at risk Yes

Parasite species

Disease in humans

Trichinella spiralis

Yes

Other Trichinella spp. Yes

Yes

Trypanosoma cruzi

Yes [49–52] Little data

Yes [49–52] Imported cases in Europe (underdiagnosed) – particularly countries with large Latin American communities

Yes [49–52]

Yes [48, 49]

Yes [48. 49]

Yes [1–6] 100% foodborne transmission Backyard domestic pork, horse meat, wild carnivores/ omnivores (boar, bear, walrus, etc.). Yes [6] Wild carnivorous meat. Horse meat possible (infrequent <1/300 000). Sea-mammals (walrus) in Arctic areas (freezeresistant T. nativa) Yes [48] Fresh juices

ANNEX 8 REGIONAL REPORTS

NOTES: A. Reportable infection in some European countries (incl. UK & Norway)

239

Sources used in Table A8.4.1

01. 02.

03.

04. 05. 06.

07.

08.

09. 10.

11.

12.

13.

14.

15.

16.

Murrell, K.D. & Pozio, E. 2011. Worldwide occurrence and impact of human trichinellosis, 1986–2009. Emerging Infectious Diseases, 17(12): 2194–2202. Dupouy-Camet, J. & Murrell, K.D. (editors). 2007. FAO/WHO/OIE Guidelines for the Surveillance, Management, Prevention and Control of Trichinellosis. World Organisatiion for Animal Health (OIE), Paris, France. See: http:/ /www.trichinellosis. org/uploads/FAO-WHO-OIE_Guidelines.pdf Pozio, E., Alban, L., Boes, J. and 19 others. 2010. Development of harmonised schemes for the monitoring and reporting of Trichinella in animals and foodstu s in the European Union. Scienti c Report submitted to EFSA. 47 p. Available at http:/ / www.efsa.europa.eu/en/supporting/doc/35e.pdf Orlandi, P.A., Chu, D.-M.T., Bier, J.W. & Jackson, G.J. 2002. Parasites and the food supply. Food Technology, 56(4): 72–81. Sli o,T.R., Smith, H.V. & Rose, J.B. 2000. Emerging parasite zoonoses associated with water and food. International Journal for Parasitology, 30: 1379–1393. Alban. L., Pozio, E., Boes, J., and 19 others. 2011. Towards a standardised surveillance for Trichinella in the European Union. Preventive Veterinary Medicine, 99(2-4): 148–160. Dorny. P., Vallée, I. Alban, L., and 18 others. 2010. Development of harmonised schemes for the monitoring and reporting of Cysticercus in animals and foodstu s in the European Union. Scienti c Report submitted to EFSA. 30 p. Available at: http:/ / www.efsa.europa.eu/en/supporting/doc/34e.pdf K.D. Murrell, P. Dorny, A. Flisser, S. Geerts, N.C. Kyvsgaard, D.P. McManus, T.E. Nash & Z.S. Pawłowski (editors). 2005. WHO/FAO/OIE Guidelines for the Surveillance, Prevention and Control of Taeniosis/Cysticercosis. OIE (World Organisation for Animal Health), Paris, France. See: p:/ / p.fao.org/docrep/ fao/011/aj005e/aj005e.pdf Torgerson, P.R. & Macpherson, C.N. 2011. The socio-economic burden of parasitic zoonoses: global trends. Veterinary Parasitology, 182(1): 79–95. Lovadina, J. 2012. La cysticercose: parasitose négligée mais véritable enjeu de santé publique dans les pays en développement. These du Docteur en Pharmacie. Faculte de Pharmacie de Grenoble, France. Halos, L. Thebault, A., Aubert, D., and 10 others. 2012. An innovative survey underlining the signi cant level of contamination by Toxoplasma gondii of ovine meat consumed in France. International Journal of Parasitology, 40: 193–200. Villena, I., Durand, B., Aubert, D., and 9 others. 2012. New strategy for the survey of Toxoplasma gondii in meat for human consumption. Veterinary Parasitology, 183: 203–208. Havelaar, A.H., Haagsma, J.A., Mangen, M.J., and 8 others. 2012. Disease burden of foodborne pathogens in the Netherlands, 2009. International Journal of Food Microbiology, 156(3): 231–238. Opsteegh, M., Prickaerts, S., Frankena, K. & Evers, E.G. 2011. A quantitative microbial risk assessment for meat-borne Toxoplasma gondii infection in The Netherlands. International Journal of Food Microbiology, 150: 103–114. EFSA. 2012. Food-borne outbreaks: Parasites. pp. 270–277, in: The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2010. Scienti c Report of EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control). Available at: http:/ /www.efsa.europa.eu/en/search/doc/2597.pdf Guy, E.C., Dubey, J.P. & Hill, D.E. 2012. Toxoplasma gondii. pp. 167–188 (Chapter 6), in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers.

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17.

Boué, F., Boes, J., Boireau, P., and 18 others. 2010. Development of Harmonised Schemes for the Monitoring and Reporting of Echinococcus in Animals and Foodstu s in the European Union. Scienti c Report submitted to EFSA. 41 p. Available at: http:/ /www.efsa.europa.eu/en/supporting/doc/36e.pdf N : for Echinoccocus (non-European species), see Table C, pp. 35–36. Takumi, K., Hegglin, D., Deplazes, P., Gottstein, B., Teunis, P. & van der Giessen, J. 2011. Mapping the increasing risk of human alveolar echinococcosis in Limburg, The Netherlands. Epidemiology and Infection, 7: 1–5. Davidson, R.K., Romig, T., Jenkins, E., Tryland, M. & Robertson, L.J. 2012. The impact of globalization on distribution of Echinococcus multilocularis. Trends in Parasitology, 28(6): 239–247. VKM (Vitenskapskomiteen for mattrygghet). 2012. Assessment of risk of introduction of Echinococcus multilocularis to mainland Norway. Opinion of the Panel on biological hazards of the Norwegian Scienti c Committee for Food Safety. Prepared by L. Robertson, J. Lassen, M. Tryland and R.K. Davidson. Doc. 11-106- nal. See: http:/ /www.vkm.no/dav/d35674e4f0.pdf Kern, P., Ammon, A., Kron, M., Sinn, G., Sander, S., Petersen, L.R., Gaus, W. & Kern, P. 2004. Risk factors for alveolar echinococcosis in humans. Emerging Infectious Diseases, 10(12): 2088–2093. Romig, T., Dinkel, A. & Mackenstedt, U. 2006. The present situation of echinococcosis in Europe. Parasitology International, 55 (Suppl): S187–S191. Schweiger, A., Ammann, R.W., Candinas, D., and 11 others. 2007. Human alveolar echinococcosis a er fox population increase, Switzerland. Emerging Infectious Diseases, 13(6): 878–882. Eckert, J. & Deplazes, P. 2004. Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews, 17(1): 107–135. Portier, J., Jouet, D., Ferte, H., Gibout, O., Heckmann, A., Boireau, P. & Vallee, I. 2012. New data in France on the trematode Alaria alata (Goeze, 1792) obtained during Trichinella inspections. Parasite-Journal de la Societe Francaise de Parasitologie, 18(3): 271–275. Portier, J., Jouet, D., Vallee, I. & Ferte, H. 2012. Detection of Planorbis planorbis and Anisus vortex as rst intermediate hosts of Alaria alata (Goeze, 1792) in natural conditions in France: Molecular evidence. Veterinary Parasitology, 190(1-2): 151–158. Taylor, M.A., Boes, J., Boireau, P., and 17 others. 2012. Development of harmonised schemes for the monitoring and reporting of Sarcocystis in animals and foodstu s in the European Union. Scienti c Report submitted to EFSA. Rosenthal, B., Yang, Z. & Yuan, L.K. 2012. Sarcocystis spp. pp. 151–166 (Chapter 5), in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers. Gardiner, C.H., Dyke, J.W. & Shirley, S.F. 1984. Hepatic granuloma due to a nymph of Linguatula serrata in a woman from Michigan: a case report and review of the literature. American Journal of Tropical Medicine and Hygiene, 33(1): 187–189. Buslau, M., Kühne, U. & Marsch, W.C. 1990. Dermatological signs of nasopharyngeal linguatulosis (halzoun, Marrara syndrome) – the possible role of major basic protein. Dermatologica, 181(4): 327. EFSA. 2012. Food-borne outbreaks: Parasites. pp. 357–358, in: The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2010. Scienti c Report of EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control). Available at: http:/ /www.efsa.europa.eu/en/search/doc/2597.pdf

18.

19.

20.

21.

22. 23.

25.

26.

27.

28.

29.

30.

31.

32.

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33.

34.

35.

36.

37.

38.

39.

40.

41.

42.

43.

44. 45.

46.

47.

EC (European Commission). 1998. Opinion of the Scienti c Committee on Veterinary Measures Relating to Public Health - Allergic reactions to ingested Anisakis simplex antigens and evaluation of the possible risk to human health. pp. 1–5. The European Commission, Health and Consumer Protection. See http:/ /ec.europa.eu/food/fs/ sc/scv/out05_en.html EFSA (European Food Safety Authority). 2011. Scienti c Opinion on assessment of epidemiological data in relation to the health risks resulting from the presence of parasites in wild caught sh from shing grounds in the Baltic Sea. EFSA Journal, 9(7): 2320 [40 p.]. Jackson, Y., Pastore, R., Sudre, P., Loutan, L. & Chappuis, F. 2007. Diphyllobothrium latum outbreak from marinated raw perch, Lake Geneva, Switzerland. Emerging Infectious Diseases, 13(12): 1957–1958. Arizono, N., Yamada, M., Nakamura-Uchiyama, F. & Ohnishi, K. 2009. Diphyllobothriasis associated with eating raw paci c salmon. Emerging Infectious Diseases, 15(6): 866–870. Scholz, T., Garcia, H.H., Kuchta, R. & Wicht, B. 2009. Update on the human broad tapeworm (genus Giphyllobothrium), including clinical relevance. Clinical Microbiology Reviews, 22(1): 146–160. Wielinga, P.R., de Vries, A., van der Goot, T.H., Mank, T., Mars, M.H., Kortbeek, L.M. & van der Giessen, J.W. 2008. Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands. International Journal of Parasitology, 38(7): 809–817. de Wit, M.A., Koopmans, M.P., Kortbeek, L.M., van Leeuwen, N.J., Bartelds, A.I. & van Duynhoven, Y.T. 2001. Gastroenteritis in sentinel general practices, The Netherlands. Emerging Infectious Diseases, 7(1): 82–91. de Wit, M.A., Koopmans, M.P., Kortbeek, L.M., Wannet, W.J., Vinje, J., van Leusden, F., Bartelds, A.I. & van Duynhoven, Y.T. 2001. Sensor, a population-based cohort study on gastroenteritis in the Netherlands: incidence and etiology. American Journal of Epidemiology, 154: 666–674. Elwin, K., Had eld, S.J., Robinson, G. & Chalmers, R.M. 2012. The epidemiology of sporadic human infections with unusual cryptosporidia detected during routine typing in England and Wales, 2000–2008. Epidemiology and Infection, 140(4): 673– 683. Robertson, L.J. & Fayer, R. 2012. Cryptosporidium spp. pp. 33–64 (Chapter 2), in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers. Vijgen, S.M.C., Mangen, M.J.M., Kortbeek, L.M., van Duijnhoven, Y.T.H.P. & Havelaar, A.H. 2007. Disease burden and related costs of cryptosporidiosis and giardiasis in the Netherlands. National Institute for Public Health and the Environment (RIVM) report 330081001/2007. Anon[ymous]. 2005. A European network for the detection and control of Cryptosporidium. MVN News, October 2005: 4. ECDC (European Centre for Disease Prevention and Control). 2011. Giardiasis. pp. 87–89, in: Annual epidemiological report. Reporting on 2009 Surveillance Data and 2010 Epidemic Intelligence Data. European Centre for Disease Prevention and Control (ECDC), Sweden. Cook, N. & Lim, Y.A.L. 2012. Giardia duodenalis. pp. 107–132 (Chapter 4), in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers. Shields, J. & Ortega, Y.R. 2012. Cyclospora cayetanensis. pp. 65–104 (Chapter 3), in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers.

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48.

49 50.

51.

52.

53. 54. 55.

56.

57.

Pereira, K.S., Barbosa, R.L., Passos, L.A.C., de Aguiar, F.S., Rogez, H., Alarcón de Noya, B. & González, O.N. 2012. Trypanosoma cruzi. pp. 189–216 (Chapter 7), in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers. Schmunis, G.A. & Yadon, Z.E. 2010. Chagas disease: a Latin American health problem becoming a world health problem. Acta Tropica, 115(1-2): 14–21. Llenas-García, J., Hernando, A., Fiorante, S., Maseda, D., Matarranz, M., Salto, E., Rubio, R. & Pulido, F. 2012. Chagas disease screening among HIV-positive Latin American immigrants: an emerging problem. European Journal of Clinical Microbiology and Infectious Disease, 31(8): 1991–1997. Pérez-Molina, J.A., Norman, F. & López-Vélez, R. 2012. Chagas disease in nonendemic countries: epidemiology, clinical presentation and treatment. Current Infectious Disease Reports, 14(3): 263–274. Sandahl, K., Botero-Kleiven, S. & Hellgren, U. 2011. [Chagas’ disease in Sweden – great need of guidelines for testing. Probably hundreds of seropositive cases, only a few known] [In Swedish]. Lakartidningen. 108(46): 2368–2371. Keiser, J. & Utzinger, J. 2005. Emerging foodborne trematodiasis. Emerging Infectious Disease, 11(10): 1507–1514. Rojas Rivero, L., Vazquez, A., Domenech, I. & Robertson, L.J. 2010. Fascioliasis: can Cuba conquer this emerging parasitosis? Trends in Parasitology, 26: 26–34 Zukiewicz, M., Kaczmarski, M., Topczewska, M., Sidor, K. & Tomaszewska, B.M. 2011. Epidemiological and clinical picture of parasitic infections in the group of children and adolescents from north-east region of Poland. Wiad Parazytol., 57(3): 179–187 Pinelli, E., Herremans, T., Harms, M.G., Hoek, D. & Kortbeek, L.M. 2011. Toxocara and Ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the Netherlands: trends from 1998 to 2009. European Journal of Clinical Microbiology and Infectious Disease, 30(7): 873–879. Albajar-Vinas, P. & Jannin, J. 2011. The hidden Chagas disease burden in Europe. EuroSurveillance, 16(38). pii: 19975.

TABLE A8.4.2 Data availability for Europe for parasite prevalence or concentration in the main food categories Anisakis spp. Seafood Yes if unfrozen Ascaris [12] Fruits Yes Vegetables Yes Cryptosporidium parvum (zoonotic); Cryptosporidium hominis (mainly anthroponotic), other Cryptosporidium spp. Dairy Milk has been associated with outbreaks – no survey data Seafood Yes [5, 10, 11] Shell sh. Fruits Yes [5, 12–15] Vegetables Yes [5, 12–15] Other Water – considerable data available from a range of sources Cyclospora cayetanensis [12, 18] Fruits Yes Vegetables Yes

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Diphyllobothrium latum and Diphyllobothrium spp. [8, 9] Seafood Yes Echinococcus granulosus (E. granulosus is transmitted to humans via eggs in dog faeces. However the occurrence of E. granulosus in slaughter animals is an important part of the transmission cycle, and thus the prevalence of E. granulosus infection in these food animals is of relevance.) Beef No data as a food vehicle Pork No data as a food vehicle Game No data as a food vehicle Fruits Yes – little data available Vegetables Yes – little data available Other Water – little data available Echinococcus multilocularis Fruits Yes – little data available Vegetables Yes – little data available Other Water – little data available Giardia duodenalis (syn. G. lamblia, G. intestinalis) Seafood Yes [5, 11, 16] Shell sh. Fruits Yes [12–14, 17] Vegetables Yes [12–14, 17] Other Water – considerable data available from a range of sources. Sarcocystis bovihominis [6,7] Beef Yes Sarcocystis suihominis [6,7] Pork Yes Taenia saginata Beef Yes Taenia solium Pork Yes. Eastern European countries or illegally imported meat. Toxoplasma gondii Beef Yes [1] Dairy Yes [1] In meat of dairy cattle, but not in milk. Pork Yes. Mainly outdoor pigs. Poultry Yes, but not relevant. Game Yes [1] Regional in wild boar. Seafood Possible. Sea mammals can be infected too. Data limited. [5] Fruits Yes [2] Vegetables Yes [2] Other Lamb and mutton; water [1–3] Trichinella spiralis Pork Yes. Outdoor pigs, pig breeding in area of high endemicity. Game Yes (wild boar and other game). Other Horse meat <1/300 000 carcasses.

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Other Trichinella species T. nativa – freeze resistant, important for game and sea mammals. T. britovi and T. murelli also important. Pork Yes Outdoor pigs, pig breeding in area of high endemcity. Game Yes (wild boar, bears). Seafood Sea mammals (seals, walrus). Other Horse meat <1/300 000 carcasses. Main Sources used in Table A8.4.2 01. Opsteegh, M., Teunis, P., Mensink, M., Züchner, L., Titilincu, A., Langelaar, M. & van der Giessen, J. 2010. Evaluation of ELISA test characteristics and estimation of Toxoplasma gondii seroprevalence in Dutch sheep using mixture models. Preventive Veterinary Medicine, 96(3-4): 232–240. Guy, E.C., Dubey, J.P. & Hill, D.E. 2012. Toxoplasma gondii. pp 167–188, in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers. Halos, L., Thebault, A., Aubert, D. and 10 others. 2010. An innovative survey underlining the signi cant level of contamination by Toxoplasma gondii of ovine meat consumed in France. International Journal for Parasitology, 40(2): 193–200. Robertson, L.J. 2007. The potential for marine bivalve shell sh to act as transmission vehicles for outbreaks of protozoan infections in humans: A review. International Journal of Food Microbiology, 120(3): 201–216. Taylor, M.A., Boes, J., Boireau, P. and 17 others. 2012. Development of harmonised schemes for the monitoring and reporting of Sarcocystis in animals and foodstu s in the European Union. Scienti c Report submitted to EFSA. 28 p. Available at http:/ /www.efsa.europa.eu/en/ supporting/doc/33e.pdf Rosenthal, B., Yang, Z. & Yuan, L.K. 2012. Sarcocystis spp. pp. 151–166, in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers. Scholz, T., Garcia, H.H., Kuchta, R. & Wicht, B. 2009. Update on the human broad tapeworm (genus Diphyllobothrium), including clinical relevance. Clinical Microbiology Reviews, 22(1): 146–160. Regional

02.

Global with regional foci Regional

03.

05.

Global problem Regional problem

06.

07.

Global problem Global with regional foci

08.

09.

EFSA [European Food Safety Authority]. 2011. Scienti c Opinion on Regional assessment of epidemiological data in relation to the health risks resulting from the presence of parasites in wild caught sh from shing grounds in the Baltic Sea. Prepared by EFSA Panel on Biological Hazards (BIOHAZ). EFSA Journal, 9(7): Art. No. 2320 [40 p.]. Robertson, L.J. & Fayer, R. 2012. Cryptosporidium spp. pp. 33–64, in: Global with L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. regional foci Nova Science Publishers. Robertson, L.J. & Gjerde, B. 2008. Development and use of a pepsin digestion method for analysis of shell sh for Cryptosporidium oocysts and Giardia cysts. Journal of Food Protection, 71(5): 959–966. Robertson, L.J. & Gjerde, B. 2001. Occurrence of parasites on fruits and vegetables in Norway. Journal of Food Protection, 64(11): 1793–1798. Amorós, I., Alonso, J.L. & Cuesta, G. 2010. Cryptosporidium oocysts and Giardia cysts on salad products irrigated with contaminated water. Journal of Food Protection, 73(6): 1138–1140. Regional

10.

11.

12. 13.

Regional Regional

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245

14.

Di Benedetto, M.A., Cannova, L., Di Piazza, F., Amodio, E., Bono, F., Cerame, G. & Romano, N. 2007. Hygienic-sanitary quality of readyto-eat salad vegetables on sale in the city of Palermo (Sicily). Igiene e Sanita Pubblica, 63(6): 659–670. Rzezutka, A., Nichols, R.A., Connelly, L., Kaupke, A., Kozyra, I., Cook, N., Birrell, S. & Smith, H.V. 2010. Cryptosporidium oocysts on fresh produce from areas of high livestock production in Poland. International Journal of Food Microbiology, 139(1-2): 96–101. Gomez-Couso, H. & Ares-Mazas, E. 2012. Giardia duodenalis. Contamination of bivalve molluscs. pp. 133–150, in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers. Cook, N. & Lim, Y.A.L. 2012. Giardia duodenalis. pp. 107–132, in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers.

Regional

15.

Regional

16.

Global with regional foci

17.

Global with regional foci

TABLE A8.4.3 Data availability for risk management options for each of parasite-commodity combinations NOTE: The authors were asked to consider all combinations of the particular parasite and the main food categories, namely Beef, Dairy, Pork, Poultry, Game, Seafood, Fruit, Vegetables and Other.

Ascaris suum Pork Yes – qualitative assessment [5] Cryptosporidium Vegetables Yes – quantitative & semi-quantitative [15–17] Other Water [11–14] Cyclospora cayetanensis – No data Fish parasites (Anisakis) Seafood Yes [18] Qualitative risk analysis Giardia duodenalis Vegetables Yes [16, 17] Quantitative & semi-quantitative Other Water [14] Taenia solium, Taenia saginata Game Qualitative risk analysis for the pork freezing [4] Toxoplasma spp. [5, 8–10] Beef yes Dairy yes Pork yes Game yes Trichinella spiralis [1–6] Pork No data, GIS mapping in the USA. [1] Qualitative risk analysis for pork freezing [4]

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Sources cited in Table A8.4.3 01. Burke, R., Masuoka, P. & Murrel, D. 2008. Swine Trichinella infection and geographic information system tools. Emerging Infectious Diseases, 14: 1109–1111. Takumi, K., Teunis, P., Fonville, M., Vallee, I., Boireau, P., Nöckler, K. & van der Giessen, J. 2009. Transmission risk of human trichinellosis. Veterinary Parasitology, 159(3-4): 324–327. Teunis, P.F., Koningstein, M., Takumi, K. & van der Giessen, J.W. 2011. Human beings are highly susceptible to low doses of Trichinella spp. Epidemiology and Infection, 14: 1–9. Regional

02.

Regional

03.

Regional

04.

Regional EFSA [European Food Safety Authority]. 2004. Opinion of the Scienti c Panel on Biological Hazards on “the suitability and details of freezing methods to allow human consumption of meat infected with Trichinella or Cysticercus”. EFSA Journal, 142: 1–50. Online; doi:10.2903/j.efsa.2005.142. EFSA [European Food Safety Authority]. 2011. Scienti c Opinion on assessment of epidemiological data in relation to the health risks resulting from the presence of parasites in wild caught sh from shing grounds in the Baltic Sea. Prepared by EFSA Panel on Biological Hazards (BIOHAZ). EFSA Journal, 9(7): Art. No. 2320 [40 p.]. Pozio, E., Alban, L., Boes, J. and 19 others. 2010 Development of harmonised schemes for the monitoring and reporting of Trichinella in animals and foodstu s in the European Union. Scienti c Report submitted to EFSA. 47 p. Available at http:/ /www.efsa.europa.eu/en/supporting/ doc/35e.pdf Opsteegh, M., Langelaar, M., Sprong, H., den Hartog, L., De Craeye, S., Bokken, G., Ajzenberg, D., Kijlstra, A. & van der Giessen, J. 2010. Direct detection and genotyping of Toxoplasma gondii in meat samples using magnetic capture and PCR. International Journal of Food Microbiology, 139(3): 193–201. Opsteegh, M., Prickaerts, S., Frankena, K. & Evers, E.G. 2011. A quantitative microbial risk assessment for meat-borne Toxoplasma gondii infection in The Netherlands. International Journal of Food Microbiology, 150(2-3): 103–114. Bayarri, S. Gracia, M.J., Lázaro, R., Pérez-Arquillué, C. & Herrera, A. 2012. Toxoplasma gondii in Meat and Food Safety Implications - A Review. Chapter 13, in: J. Lorenzo-Morales (editor). Zoonosis. Online publ. by InTech. See: http:/ /www.intechopen.com/books/zoonosis Pouillot, R., Beaudeau, P., Denis, J.B. & Derouin, F. 2004. A quantitative risk assessment of waterborne cryptosporidiosis in France using secondorder Monte Carlo simulation. Risk Analysis, 24: 1–17. WHO. 2009. Risk assessment of Cryptosporidium in drinking-water. WHO doc. no. WHO/HSE/WSH/09.04 See: http:/ /www.who.int/water_ sanitation_health/publications/cryptoRA/en/ Regional

05.

06.

Regional

07.

Regional

08.

Regional

10.

Global

11.

Regional

12.

Regional

13.

Regional Cummins, E., Kennedy, R., Cormican, M. 2010. Quantitative risk assessment of Cryptosporidium in tap water in Ireland. Science of The Total Environment, 408(4): 740–753. Hunter, P.R., de Sylor, M.A., Risebro, H.L., Nichols, G.L., Kay, D. & Hartemann, P. 2011. Quantitative microbial risk assessment of cryptosporidiosis and giardiasis from very small private water supplies.Risk Analysis, 31(2): 228–236. Regional

14.

15.

Global Grace, D., Monda, J., Karanja, N., Randolph, TF. & Kang’ethe, E.K. 2012. Participatory probabilistic assessment of the risk to human health associated with cryptosporidiosis from urban dairying in Dagoretti, Nairobi, Kenya. Tropical Animal Health and Production, 44(Suppl.1): S33–S40. doi: 10.1007/s11250-012-0204-3.

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16.

Mota, A., Mena, K.D., Soto-Beltran, M., Tarwater, P.M. & Cháidez, C. 2009. Risk assessment of Cryptosporidium and Giardia in water irrigating fresh produce in Mexico. Journal of Food Protection, 72(10): 2184–2188. Robertson, L.J., Greig, J.D., Gjerde, B. & Fazil, A. 2005. The potential for acquiring cryptosporidiosis or giardiosis from consumption of mung bean sprouts in Norway: a preliminary step-wise risk assessment. International Journal of Food Microbiology, 98(3): 291–300. EFSA [European Food Safety Authority]. 2010. Panel on Biological Hazards (BIOHAZ), 2010. Scienti c Opinion on risk assessment of parasites in shery products. EFSA Journal, 8: 91 [33 p]

Global

17.

Regional

18.

Regional

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ANNEX 8.5 NEAR EAST A8.5.1 Compilation of data availability on food borne parasites relevant to the Near East e group comprised Mohammad B. Rokni, Islamic Republic of Iran; Said Shalaby, Egypt; and Darwin Murrell, Denmark (who acted as group leader). e region was subdivided into three groups of countries and each assigned to the group member with the greatest experience with the particular area. A er review of the literature covering all those parasites that had been reported from the area, the group selected those parasites for which a reasonable amount of data was available, and these are listed below and in the three tables. A er compiling the tables, the group then wrote this report that summarizes the information displayed in the tables, and o ers opinion on research gaps and relative importance of the parasites listed. e group selected the following parasites to be given priority: • Ascaris spp • Cryptosporidium parvum • Echinococcus granulosus & E. multilocularis • Entamoeba histolytica • Fasciola spp. • Giardia duo denalis (syn. G. lamblia, G. intestinalis) • Haplorchis pumilio • Heterophyes heterophyes • Taenia saginata • Toxoplasma gondii • Trichuris trichiura e prevalence of water- and foodborne parasites in the area (Enatamoeba, Cryptosporidium, Giardia and Toxoplasma) is generally high, as evident from the numerous prevalence surveys that have been conducted (Tables A8.5.1 and A8.5.2). ese parasites are also of global importance. Overall, the availability and quality of these reports is good. However, studies on disease burden (e.g. morbidity/mortality or sequelae) are generally lacking, which makes estimating very di cult. Similarly, quantitative epidemiology studies are also limited, although a few recent studies on risk factors have appeared for all of these species. For helminths, the availability of reports on prevalence is good for certain of the parasites ( e.g.,, E. granulosus—see Torgerson et al., 2010). Although data are available from hospital records, it may not be su cient to permit reliable estimates of disease burden.

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Fasciola spp. are second only to Schistosoma spp. as the most common trematode infection, especially in Egypt, Yemen and Iran, and account for more than one-third of the world’s cases of fascioliasis. As a proportion of the global burden of disease, fascioliasis, ascariasis and trichuriasis in Near East countries account for 36%, 3% and 1%, respectively, of the total global prevalence (Hotez, Savioli and Fenwick, 2012). In contrast, the prevalence of human Taenia saginata (taeniosis) is infrequently reported, as is bovine cysticercosis from meat inspection. is is in contrast to some countries in Africa. Meat inspection data, which would be valuable in estimating risk from this parasite, are not readily available, although such data might be obtained from the grey literature. Reports on the sh-borne intestinal ukes (e.g. Haplorchis pumilio and Heterophyes heterophyes) indicate that these parasites are common in the Nile Delta region of Egypt, where the food habit of eating improperly cooked sh is well established. ere are numerous prevalence and epidemiology reports on the soil-borne parasites, Ascaris spp. and Trichuris spp. ese parasites are very common throughout the region. Overall, the speci c food sources for many of the zoonotic parasites are poorly documented.

A8.5.2 Agri-food trade Normally, due to low income and geographical situation, many countries of the region are not exporters of meat and meat products; the greatest income in most of the countries is from oil. e same may also be true for exports of high-risk fruits and vegetables, but this needs further inquiry. A potential future obstacle for some countries in attempting to export beef and lamb could be bovine cysticercosis and echinococcosis. In some countries of Africa, income from export of beef is negatively a ected by bovine cysticercosis. One study on the economic impact of echinococcosis relevant to area was found (see Table A8.5.2).

A8.5.3 Consumer perception and social sensitivity ere is limited information on knowledge, attitude and behaviour of consumers related to foodborne parasites in region. In Iran there are several studies on echinococcosis, and the results show that general perception is not good. is topic has not been widely discussed in the region compared with other regions, judging by the global literature. Local awareness of parasitic disease is poor, although there are limited studies in Iran. Continued turmoil in many 250 MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

countries of the region prevents governments from raising social sensitivity on this topic, and accordingly people are not interested or aware.

A8.5.4 Risk management e strategies for the reducing the risk from foodborne parasites vary considerably, re ecting the diversity of these parasite’s life histories and their epidemiology, and so are not easily generalized. Although regional reports are few, there are numerous recommendations in the global literature, as noted in Table A8.5.3.

A8.5.5 Sources cited in the discussion Hotez, P.J., Savioli, L. & Fenwick, A. 2012. Neglected tropical diseases of the Middle East and North Africa: Review of their prevalence, distribution, and opportunities for control. PLoS Neglected Tropical Diseases, 6(2): Art. no. e1475 [Online; DOI: 10.1371/journal.pntd.0001475]. Torgerson, P.R., Keller, K., Magnotta, M. & Ragland, N. 2010. e global burden of alveolar echinococcosis. PLoS Neglected Tropical Diseases, 4(6): Art. no. e722 [Online; DOI: 10.1371/journal.pntd.0000722].

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252 Global level Main food source and attribution Yes Disease in humans Main food sources and attributions Disease severity/main population at risk Yes [10, 44–52] No Yes Nearly all studies have Contaminated salad data on this topic in the region Yes [8, 14,19, 35–43] Yes Water, some transmission by contaminated plant material. Yes Considerable data from hospital and clinic records Disease severity/main population at risk Yes [53, 54] Poor children in tropical countries, with overcrowded slums and inadequate sanitation Yes Vegetables washed with contaminated water Yes [58] shepherds followed by farmers No data Multiple sources. Yes [25, 59–70] Yes [25, 59–70] Hydatid cysts are very serious and di cult to treat. Yes Man is an intermediate host, and likely is infected by ingestion of eggs in contaminated soil and water.

TABLE A8.5.1 Data availability on food borne parasites relevant to the Near East

Data availability on human disease related parameters Regional level

Parasite species

Disease in humans

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Yes [10, 44–55] Saudi Arabia – 0.4–22.2%; Iran – 0.57–1.5%; Qatar – 0.6%; UAE – 6.6%; Egypt – 23%; Libya – 0.1%; Sudan – 47.7% Cryptosporidium Yes [8, 14,19, 35–43] Reported human prevalence: parvum Gaza - 16.3%; Jordan - 8.3%; Yemen - 24–44%; Saudi Arabia – 2.3–16%; Iraq – 5–9.7%; Kuwait – 3.4%; Egypt – 9% Libya – 2.5% Sudan – 16%. Echinococcus Yes [58] Iraq – 2/100 000; granulosus. Iran – 0.6-1.2/100 000 and prevalence 1.2–24%; Yemen – 26–140 cases/year during 2001–2008; Egypt – 10%; Libya – 1.4%; Sudan – 0.5%.

Ascaris lumbricoides

Data availability on human disease related parameters Regional level Global level Main food source and attribution No data Epidemiological studies on major source inadequate to determine. Yes Disease in humans Disease severity/main population at risk Yes [1–9] Nearly all studies have data on this topic in the region

Parasite species

Disease in humans

Entamoeba. histolytica

Disease severity/main Main food sources population at and attributions risk Yes Vegetables, water and soil. Relative importance of water- or foodborne uncertain; may vary in di erent circumstances.

Fasciola spp.

Yes [1–9] Reported human prevalence ranges: Lebanon– 14.0–19.5%; Gaza – 70%; Jordan – 22–80%; Syria – 22%; Yemen – 17%; Saudi Arabia – 0.14–30.3%; Iran – 1–9%; Oman – 0.5–2.4%; Qatar – 0.12%; Egypt >21%; Libya – 4.2%; Sudan – 54% Yes [44, 72–76] Iran: – >7000 (1989) & 10 000 (1999) cases in massive outbreaks in north, and 17 cases in Iran in Kermanshah outbreak. Now less than 0.1%. Egypt has most prevalence (2.8%), followed by Yemen and Iran Yes [44, 72–76] Iran and Egypt. In Iran there are considerable data. Yes [44, 72–76] Yes [44, 72–76] Yes [71, 76] Yes [72–74, 85] Two waterplants – Nasturtium microphyllum and Mentha longifolia Watercress (local name boolagh oti) contaminated with Fasciola metacercariae Mentha pulegium (local name khlivash) and Mentha piperita (local name bineh)

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254 Global level Main food source and attribution Yes [24] Probably mostly waterborne. Fish Yes Disease in humans Disease severity/main Main food sources population at and attributions risk Yes Yes Children have especially high prevalence Disease severity/main population at risk Yes [1, 3, 6, 8, 10–24] Bakery workers [82] Nearly all studies have data on this topic in the region Yes [45, 57, 58] Yes Common in shers, Fish meat (esp. and others consuming uncooked) improperly cooked sh. Yes Yes Improperly cooked sh

Data availability on human disease related parameters Regional level

Parasite species

Disease in humans

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Giardia duodenalis (syn. G. lamblia, G. intestinalis)

Intestinal shborne trematodes Heterophyes heterophyes H. nocens Haplorchis pumilio

Yes [1, 3, 6, 8, 10–24] Reported human prevalence ranges: Jordan – 3.9–42.6%; Gaza – 10.3–62.2%; Lebanon – 20.7%; West Bank – 9,7%; Syria – 14.0–31.0%; Yemen – 19.7%; Saudi Arabia – 0.1–37.7%; Iran – 3.7–14.5%; Oman – 3.4–10.5%; Qatar – 1.6%; Bahrain – 4%; Iraq – 38.5%; Egypt – 42%; Libya – 1.7%; Sudan – 12.3%. Yes [45, 57, 58] Hyperendemic, especially in delta region of the Nile Egypt – 33.8%; Iran – 0.24%; Sudan – 11%.

Data availability on human disease related parameters Regional level Global level Main food source and attribution Yes, beef. No data Disease in humans Disease severity/main population at risk No data Disease severity/main Main food sources population at and attributions risk Yes beef

Parasite species

Disease in humans

Taenia saginata [12, 16,

77–81]

Toxoplasma gondii

Yes Human prevalence in the region 0.4 and 6.0% in the few studies reported. Saudi Arabia – 0.01–0.2%; Iran – 0.1%; Qatar – 0.4%; Egypt – 0.6%; Libya – 2%; Sudan – 0.9%. Yes [26–34] Human prevalence: Lebanon – 62%; Saudi Arabia – 3.78–4.9% and 42.3%; Qatar – 29.8%; Bahrain – 4%; Egypt – 11.7%; Libya – 43.4%; Sudan – 44.4%. Yes [26–34] Nearly all studies have data on this topic in the region Yes [26–34] Yes [25] However, direct ingestion of oocysts disseminated by infected cats are also important risk [83, 84] Toxoplasma gondii DNA was detected in 25% of salami, 20.3% of sausage, 21.8% of hamburger and 32.8% of kebab [29] No data Yes Yes [25] Yes Pork, lamb.

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Trichuris trichiura

Yes [1, 10, 46, 55–57] Saudi Arabia – 0.36–28.8%; Qatar – 26.3%; UAE – 6.2%; Egypt – 49.7% Sudan – 46%.

Yes [1, 10, 46, 56, 57] Nearly all studies have data on this topic in the region

Yes

255

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02.

03.

04.

06.

07.

08. 09. 10.

12.

13. 14. 15.

16.

17. 18.

19.

20. 21. 22.

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MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

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27.

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35.

36. 37.

38. 39. 40. 41.

42. 43.

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47.

48.

49.

50. 51. 52. 53.

54. 55.

56.

57.

58. 58. 59.

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66.

67.

68.

69.

70. 71.

72.

72. 73.

75.

76.

77.

78.

79.

80.

81.

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259

82.

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83.

84. 85.

TABLE A8.5.2 Data availability for parasite prevalence or concentration in the main food categories in the Near East Ascaris lumbricoides Fruits Vegetables Other Via municipal recycling of waste-water in farming. Yes [3, 34] Via municipal re-cycling of waste-water in crops. Accidental ingestion of mature Ascaris eggs through contaminated food or water.

Cryptosporidium parvum [6,22] Fruits Vegetables Other Yes. If contaminated with water containg oocysts Yes. As for fruit. Mostly waterborne.

Echinococcus granulosus [30] Fruits Vegetables Other Yes [32] Yes [31, 33] The eggs may be eaten in foods (e.g. vegetables, fruits or herbs, or drunk in contaminated water

Entamoeba hystolytica Fruits Vegetables Other Yes 2, 4] Yes [1–3] Water [1-2]

Fasciola spp. [23–25] Vegetables Other Yes [3, 26} Primarily leafy greens raised in water (ponds, streams). Some infective stages (metacercariae) may be transmitted by water.

Fish-borne trematodes Seafood Ingestion of improperly cooked fresh and brackish-water sh Giardia duodenalis (syn. G. lamblia, G. intestinalis) Fruits Vegetables Other Yes [10] Yes [1, 5–7] Yes [1, 5–9] Water, sh.

260

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Taenia saginata [27–28] Beef Yes Toxoplasma gondii Beef Dairy Pork Poultry Game Fruits Vegetables Other Yes [17] Yes [15–16] Yes [11–14] Yes [19] Yes Yes [20] Yes [11–14] When cat faeces deposited in vegetable farm. Yes [11–14, 18] Soil and water; pork and oocyst contaminated water, fruits and vegetables have been implicated; T. gondii DNA was detected in 25% of salami, 20.3% of sausage, 21.8% of hamburger and 32.8% of kebab samples. [18]

Sources cited for Table A8.5.2 01. Baldursson, S. & Karanis, P. 2011. Waterborne transmission of protozoan parasites: Review of worldwide outbreaks – An update 2004–2010. Water Research, 45(20): 6603–6614. Ximenez, C., Moran, P., Rojas, L., Valadez, A. & Gomez, A. 2009. Reassessment of the epidemiology of amebiasis: State of the art. Infection Genetics and Evolution, 9(6):1023–1032. Daryani, A., Ettehad, G.H., Sharif, M., Ghorbani, L. & Ziaei, H. 2008. Prevalence of intestinal parasites in vegetables consumed in Ardabil, Iran. Food Control, 19(8): 790–794. Information from http:/ /www.medic8.com/healthguide/food-poisoning/ entamoeba-histolytica.html Rionda, Z.L. & Clements, A. 2005. The burden of disease in West Bank and Gaza: An assessment Report. 27 p. Report sumitted to the US AID, MEDS Project Contract No. HRN-I-00-99-00002-00. MEDS Publications, Washington D.C., USA. Hunter, P.R. & Thompson, R.C.A. 2005. The zoonotic transmission of Giardia and Cryptosporidium. International Journal for Parasitology, 35(1112): 1181–1190. Alyouse , N.A., Mahdy, M.A.K., Mahmud, R. & Lim, Y.A.L. 2011. Factors associated with high prevalence of intestinal protozoan infections among patients in Sana’a City, Yemen. PLoS ONE, 6(7): Art. no. e22044. [Online; DOI: 10.1371/journal.pone.0022044] Ghoneim, N.H., Abdel-Moein, K.A. & Saeed, H. 2012. Fish as a possible reservoir for zoonotic Giardia duodenalis assemblages. Parasitology Research, 110(6): 2193–2196. Al-Binali, A.M., Bello, C.S., El-Shewy, K. & Abdulla, S.E. 2006. The prevalence of parasites in commonly used leafy vegetables in south-western Saudi Arabia. Saudi Medical Journal, 27(5): 613–616. Anon. No date. [Giardiasis fact sheet] Online. See: http:/ /medicalcenter. osu.edu/patientcare/healthcare_services/infectious_diseases/giardiasis/ Pages/index.aspx Global

02.

Global

03.

Global with regional foci Global Global

04. 05.

06.

Global

07.

Global

08.

Global

09.

Regional

10.

Global

ANNEX 8 REGIONAL REPORTS

261

11.

Torgerson, P.R. & Macpherson, C.N.L. 2011. The socioeconomic burden of parasitic zoonoses: Global trends. Veterinary Parasitology, 182(1; Special issue): 79–95. Dubey, J.P. 2004. Toxoplasmosis – a waterborne zoonosis. Veterinary Parasitology, 126(1-2; Special Issue): 57–72.

Global

12. 13.

Global

Global Alvarado-Esquivel, C., Estrada-Martinez, . & Liesenfeld, O. 2011. Toxoplasma gondii infection in workers occupationally exposed to unwashed raw fruits and vegetables: a case control seroprevalence study. Parasites & Vectors, 4: Art. No. 235. [Online; DOI: 10.1186/1756-3305-4-235] Lass, A., Pietkiewicz, H., Szostakowska, B. & Myjak, P. 2012. The rst detection of DNA in environmental fruits and vegetables samples. European Journal of Clinical Microbiology & Infectious Diseases, 31(6): 1101–1108. Tzanidakis, N., Maksimov, P., Conraths, F.J., Kiossis, E., Brozos, C., Sotiraki, S. & Schares, G. 2012. Toxoplasma gondii in sheep and goats: Seroprevalence and potential risk factors under dairy husbandry practices. Veterinary Parasitology, 190(3-4): 340–348. Asgari, Q., Mehrabani, D., Motazedian, M.H., Kalantari, M., Nouroozi, J. & Adnani Sadati, S.J. 2011. The viability and infectivity of Toxoplasma gondii tachyzoites in dairy products undergoing food processing. Asian Journal of Animal Sciences, 5(3): 202–207. Kijlstra, A. & Jongert, E. 2008. Control of the risk of human toxoplasmosis transmitted by meat. International Journal for Parasitology, 38(12): 1359–1370. Fallah, E., Hajizadeh, M., Farajnia, S. & Khanmohammadi, M. 2011. Prevalence of Toxoplasma gondii in food products in north west of Iran in 2010. Australian Journal of Basic and Applied Sciences, 5(6): 1482–1485. Dubey, J.P. 2010. Toxoplasma gondii infections in chickens (Gallus domesticus): prevalence, clinical disease, diagnosis and public health signi cance. Zoonoses and Public Health, 57(1): 60–73. Pereira, K.S., Franco, R.M. & Leal, DA. 2010. Transmission of toxoplasmosis (Toxoplasma gondii) by foods. Advances in Food and Nutrition Research, 60: 1–19. Fayer, R. 2004. Cryptosporidium: a water-borne zoonotic parasite. Veterinary Parasitology, 126(1-2): 37–56. Global

14.

15.

Global

16.

Regional

17. 18.

Regional Regional

19.

Global

20.

Global

22. 23.

Global

Global Ashra , K., Valero, M.A., Massoud, J., Sobhani, A., SolaymaniMohammadi, S., Conde, P., Khoubbane, M., Bargues, M.D. & Mas-Coma, S. 2006. Plant-borne human contamination by fascioliasis. American Journal of Tropical Medicine and Hygiene, 75(2): 295–302. Mas-Coma, S., Valero, M.A. & Bargues, M.D. 2009. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology, 69: 41–146. Ashra , K., Valero, M.A., Forghan-Parast, K., Rezaeian, M., Shahtaheri, S.J., Hadiani, M.R., Bargues, M.D. & Mas-Coma, S. 2006. Potential transmission of human fascioliasis through traditional local foods, in northern Iran. Iranian Journal of Public Health, 35(2): 57–63. Sarkari, B., Ghobakhloo, N., Moshfea, A. & Eilami, O. 2012. Seroprevalence of human fasciolosis in a new-emerging focus of fasciolosis in Yasuj district, southwest of Iran. Iran Journal of Parasitology, 7(2): 15–20. Murrell, K.D. 2005. Epidemiology of taeniosis and cysticercosis. pp. 27–43 (Chapter 3), in: K.D. Murrell, P. Dorny, A. Flisser, S. Geerts, N.C. Kyvsgaard, D.P. McManus, T.E. Nash and Z.S. Pawłowski (editors). WHO/FAO/OIE Guidelines for the Surveillance, Prevention and Control of Taeniosis/ Cysticercosis. OIE (World Organisation for Animal Health), Paris, France. Khaniki, G.R., Raei, M., Kia, E.B., Haghi, A.M. & Selseleh, M. 2010. Prevalence of bovine cysticercosis in slaughtered cattle in Iran. Tropical Animal Health and Production, 42(2): 141–143. Global Global

24.

25.

26.

Regional

27.

28.

262

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29.

Robinson, M.W. & Dalton, J.P. 2009. Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Philosophical Transactions of the Royal Society, Series B: Biological Sciences, 364(1530): 2763–2776.

Global

30.

Global Harandi, M.F., Moazezi, S.S., Saba, M., Grimm, F., Kamyabi, H., Sheikhzadeh, F., Shari , I. & Deplazes, P. 2011. Sonographical and serological survey of human cystic echinococcosis and analysis of risk factors associated with seroconversion in rural communities of Kerman, Iran. Zoonoses and Public Health, 58(8): 582–588. Rokni, M.B. 2009. Echinococcosis/hydatidosis in Iran. Iranian Journal of Parasitology, 4(2): 1–16. Anon. 2011. Echinococcosis (Echinococciasis, Hydatidosis, Hydatid Disease) [Online Factsheet] Center for Food Security and Public Health, College of Veterinary Medicine, Iowa State University, USA. See: http:/ /www.cfsph. iastate.edu/Factsheets/pdfs/echinococcosis.pdf. Bourée, P. 2001. Hydatidosis: dynamics of transmission. World Journal of Surgery, 25(1): 4–9. Global Global

31. 32.

33. 34.

Global

Shahnazi, M. & Jafari-Sabet, M. 2010. Prevalence of parasitic contamination Regional of raw vegetables in villages of Qazvin Province, Iran. Foodborne Pathogens and Disease, 7(9): 1025–1030.

Table A8-5-3 Data availability for risk management options for each of parasite-commodity combinations in the Near East Read in close conjunction with Tables A8.5.1 and A8.5.2 NOTE: The authors were asked to consider all combinations of the particular parasite and the main food categories, namely Beef, Dairy, Pork, Poultry, Game, Seafood, Fruit, Vegetables and Other.

Ascaris lumbricoides, Trichuris trichiura The main source of infection is vegetables, so the best management would be to prevent use of night soil on vegetable farms, and improving composting techniques for manure. Fruits Vegetables Yes Yes [27]

Echinococcus granulosus Control of dog populations in endemic areas is necessary. There are possible implication for fruits and vegetables. See references 15–22. Beef Pork Game Fruits Vegetables Yes Yes Yes Yes Yes

Entamoeba hystolytica, Giardia duodenalis (syn. G. lamblia, G. intestinalis) and Cryptosporidium parvum The parasites Entamoeba, Giardia and Cryptosporidium can be grouped as primarily waterborne. Risk reduction involves the supply of potable, safe water for not only drinking, but also for food preparation and washing mouth and hands. Relevant publications linked to these parasites are in Table A8.5.2.

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Fruits Vegetables Other

Yes [1–10] Yes [1–10] Yes. All are water-borne.

Fishborne trematodes: Heterophyes heterophyes, Haplorchis pumilio, Procerovum spp. Only sh and humans are important in the control of this zoonosis. Dogs may play a role as alternative de nitive host in endemic areas. Major risk factors include the use of sh from infested regions and improper cooking, or even eating sh raw with spices. Strict sh muscle examination is needed, especially for imported sh. Deep freezing on board is mandatory for imported sh. Examination by veterinary and health authorities and application of national standards is obligatory. Seafood Fasciola spp. Risk management programmes are described in numerous publications, speci c for humans or for livestock. See references 23–24. Beef Dairy Pork Game Vegetables Taenia saginata Because of strict host speci city, only cattle and humans are important in the epidemiology and control of this zoonosis. Major risk factors include exposure of animals to faecal waste. For humans, exposure to inadequate meat inspection, inadequate cooking temperatures. Considerable information on this available in the WHO/FAO/OIE Guidelines[28]. For mitigation of risk in cattle and consumer meats, see reference 25. For control in humans and egg contamination of the environment (by cattle), see reference 26. Beef Dairy Toxoplasma gondii Recent evidence that Toxoplasma could be transmitted by contaminated fruits and vegetables is covered in references 11–14, q.v. See Table A8.5.2 for references on meat and water transmission. Risk management will require improvement in water safety as well as prevention of exposure of livestock to infected cats. Beef Dairy Pork Poultry Yes [11–14] Yes [11–14] Yes [11–14] Yes [11–14] Yes Yes? Yes Yes Yes Yes Yes Yes

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Fruits Vegetables Other

Yes [11–14] Yes [11–14] Yes [11–14]

References cited in Table A8.5.3 01. Rionda, Z.L. & Clements, A. 2005. The burden of disease in West Bank and Gaza: An assessment Report. 27 p. Report sumitted to the US AID, MEDS Project Contract No. HRN-I-00-99-00002-00. MEDS Publications, Washington D.C., USA. Sha’ar, A, Kelly, P. & Kleinau, E. 2003. USAID village water and sanitation program, West Bank of Palestine: Environmental health assessment—Phase II. Report, Environmental Health Project, Contract HRN-I-00-99-0011-00, O ce of Health, Infectious diseases and Nutrition, Bureau for Global Health, US Agerncy for International Development, Washington D.C., USA. Erickson, M.C. & Ortega, Y.R. 2006. Inactivation of protozoan parasites in food, water, and environmental systems. Journal of Food Protection, 69(11): 2786–2808. Ranjbar-Bahadori, S., Sangse di, H., Shemshadi, B. & Kashe nejad, M. 2011. Cryptosporidiosis and its potential risk factors in children and calves in Babol, north of Iran. Tropical Biomedicine, 28(1): 125–131. Stau er, W., Abd-Alla, M. & Ravdin, J.I. 2006. Prevalence and incidence of Entamoeba histolytica infection in South Africa and Egypt. Archives of Medical Research, 37(2): 266–269. Gusbi, M.M. 2007. Aetiology of acute diarrhoea in hospitalized children, Tripoli, Libya. PhD thesis, University of Salford, UK. Saeed, A., Abd, H., Evengard, B. Sandstrom, G. 2011. Epidemiology of entamoeba infection in Sudan. African Journal of Microbiology Research, 5(22): 3702–3705. Sullivan, P.S., Dupont, H.L., Arafat, R.R., Thornton, S.A., Selwyn, B.J., Elalamy, M.A. & Zaki, A.M. 1988. Illness and reservoirs associated with Giardia lamblia infection in rural Egypt – the case against treatment in developing world environments of high endemicity. American Journal of Epidemiology, 127(6): 1272–1281. Youssef, F.G., Adib, I., Riddle, M.S. & Schlett, C.D. 2008. A review of cryptosporidiosis in Egypt. Journal of the Egyptian Society of Parasitology, 38(1): 9–28. Adam, A.A., Hassan, H.S., Shears, P. & Elshibly, E. 1994. Cryptosporidium in Khartoum, Sudan. East African Medical Journal, 71(11): 745–746 Alvarado-Esquivel, C., Estrada-Martinez, . & Liesenfeld, O. 2011. Toxoplasma gondii infection in workers occupationally exposed to unwashed raw fruits and vegetables: a case control seroprevalence study. Parasites & Vectors, 4: Art. No. 235. [Online; DOI: 10.1186/1756-3305-4-235] Lass, A., Pietkiewicz, H., Szostakowska, B. & Myjak, P. 2012. The rst detection of DNA in environmental fruits and vegetables samples. European Journal of Clinical Microbiology & Infectious Diseases, 31(6): 1101–1108. Kijlstra, A. & Jongert, E. 2008. Control of the risk of human toxoplasmosis transmitted by meat. International Journal for Parasitology, 38(12): 1359–1370. Asgari, Q., Mehrabani, D., Motazedian, M.H., Kalantari, M., Nouroozi, J. & Adnani Sadati, S.J. 2011. The viability and infectivity of Toxoplasma gondii tachyzoites in dairy products undergoing food processing. Asian Journal of Animal Sciences, 5(3): 202–207. Harandi, M.F., Moazezi, S.S., Saba, M., Grimm, F., Kamyabi, H., Sheikhzadeh, F., Shari , I. & Deplazes, P. 2011. Sonographical and serological survey of human cystic echinococcosis and analysis of risk factors associated with seroconversion in rural communities of Kerman, Iran. Zoonoses and Public Health, 58(8): 582–588. Rokni, M.B. 2009. Echinococcosis/hydatidosis in Iran. Iranian Journal of Parasitology, 4(2): 1–16. El-Shazly, A.M., Awad, S.E., Hegazy, M.A., Mohammad, K.A. & Morsy, T.A. 2007. Echinococcosis granulosis/hydatosis an endemic zoonotic disease in Egypt. Journal of the Egyptian Society of Parasitology, 37(2): 609–622.

02.

03. 04

05. 06. 07. 09.

09. 10. 11.

12.

13. 14.

15.

16. 18.

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19.

Dyab, K.A., Hassanein, R., Hussein, A.A., Metwally, S.E. & Gaad, H.M. 2005. Hydatidosis among man and animals in Assiut and Aswan Governorates. Journal of the Egyptian Society of Parasitology, 35(1): 157–166. Shambesh, M.K., Macpherson, C.N.L., Beesley, W.N., Gusbi, A. & Elsonosi, T. 1992. Prevalence of human hydatid-disease in north-western Libya - a cross-sectional ultrasound study. Annals of Tropical Medicine and Parasitology, 86(4): 381–386. Magambo, J.K., Hall, C., Zeyle, E. & Wachira, T.M. 1996. Prevalence of human hydatid disease in southern Sudan. African Journal of Health Science, 3(4): 154–156. Bourée, P. 2001. Hydatidosis: dynamics of transmission. World Journal of Surgery, 25(1): 4–9. Mas-Coma, S., Bargues, M.D. & Valero, M.A. 2005. Fascioliasis and other plant-borne trematode zoonoses. International Journal of Parasitology, 35(11-12): 1255–1278. Fürst, T., Sayasone, S., Odermatt, P., Keiser, J. & Utzinger, J. 2012. Manifestation, diagnosis, and management of foodborne trematodiasis. British Medical Journal, 344(7863): Art. no. e4093. [Online; doi: 10.1136/bmj.e4093] Kyvsgaard, N. & Murrell, K.D. 2005. Prevention of taeniosis and cysticercosis. pp. 57–72, in: K.D. Murrell, P. Dorny, A. Flisser, S. Geerts, N.C. Kyvsgaard, D.P. McManus, T.E. Nash and Z.S. Pawłowski (editors). WHO/FAO/OIE Guidelines for the Surveillance, Prevention and Control of Taeniosis/Cysticercosis. OIE (World Organisation for Animal Health), Paris, France. Pawlowski, Z.S., Allan, J.C. & Meinardi, H. 2005. Control measures for taeniosis and cysticercosis. pp. 73–99 (Chapter 6), in: K.D. Murrell, P. Dorny, A. Flisser, S. Geerts, N.C. Kyvsgaard, D.P. McManus, T.E. Nash and Z.S. Pawłowski (editors). WHO/FAO/OIE Guidelines for the Surveillance, Prevention and Control of Taeniosis/Cysticercosis. OIE (World Organisation for Animal Health), Paris, France. Moro, P.L., Cavero, C.A., Tambini, M., Briceno, Y., Jimenez, R. & Cabrera, L. 2008. Identi cation of risk factors for cystic echinococcosis in a peri-urban population of Peru. Transactions of the Royal Society of Tropical Medicine and Hygiene, 102(1): 75–78. Shahnazi, M. & Jafari-Sabet, M. 2010. Prevalence of parasitic contamination of raw vegetables in villages of Qazvin Province, Iran. Foodborne Pathogens and Disease, 7(9): 1025–1030. WHO/FAO/OIE. 2005. WHO/FAO/OIE Guidelines for the Surveillance, Prevention and Control of Taeniosis/Cysticercosis. Edited by K.D. Murrell, P. Dorny, A. Flisser, S. Geerts, N.C. Kyvsgaard, D.P. McManus, T.E. Nash and Z.S. Pawłowski. OIE (World Organisation for Animal Health), Paris, France. See: p:/ / p.fao.org/docrep/fao/011/aj005e/aj005e.pdf

20.

21. 22. 23. 24.

25.

26.

27.

27. 28.

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ANNEX 8.6 NORTH AMERICA WITH NOTES ON CENTRAL AMERICA A8.6.1 Report preparation is summary of data availability on foodborne parasites relevant to the North American region was compiled by Ronald Fayer, USA; Brent Dixon, Canada; and Ynes Ortega, USA, who acted as leader. Communication via e-mail and telephone served to compile information and complete the tables used to dra this report.

A8.6.2 Data availability on human occurrences and food attribution Four parasite genera are of most importance in North America: Toxoplasma, Cryptosporidium, Cyclospora and Giardia. Data relevant to these parasites are available in published reports on cases, outbreaks, surveys and public records. ere is insu cient or lack of data from exporting countries (fresh produce, meats, sh and shell sh) and where parasites are endemic. ere was limited information on good agricultural practices, water quality, and worker hygiene (sanitation). Information that could be used for trace-back investigations is not readily available, which delays outbreak investigations. In addition, an attempt was made to identify appropriate sources from Central America. e meagre information available is summarized in Table A8.6.4.

A8.6.3 Data on the burden of disease and food attribution e data accessible has been summarized in Table A8.6.1. e estimated costs (in US dollars) of illness caused by the four pathogens of concern in North America are: Cryptosporidium ($47 million), Cyclospora ($2 million) and Toxoplasma ($2.973 billion). Toxoplasma is considered the fourth leading cause of hospitalizations (n=4428) and the second cause of deaths (n=327) associated with foodborne illnesses in the USA. Annually the estimated number of illnesses attributed to Cyclospora in the USA is 11 407, 57 616 for Cryptosporidium, 86 686 for Toxoplasma and 76 840 for Giardia. Data on parasite prevalence, incidence and concentration in the main food categories are summarized in Table A8.6.2

A8.6.4 Agri-food trade From the high-pro le Cyclospora outbreaks in North America, consumers are aware of the risks of eating fresh produce from developing countries, especially raspberries, mesclun lettuce and basil. e economic impact on producers if their food item is implicated in a foodborne outbreak is signi cant. at was the case

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of Cyclospora in 1995, where the outbreak was incorrectly attributed to California strawberries. is resulted in a $20 million loss to that industry. Outbreaks associated with Cyclospora in 1996 and 1997 caused illness in more than 2000 individuals in North America. Contaminated raspberries from Guatemala were identi ed. As result of these outbreaks, imports of Guatemalan raspberries to the USA and Canada were restricted, resulting in signi cant losses to the berry industry.

A8.6.5 Consumer perception As result of widely publicized foodborne outbreaks in North America, consumers are aware of risks associated with eating fresh produce, especially from developing countries. Washing fresh produce is common practice and thoroughly cooking or freezing of meats is common practice. Consumers expect government inspection to keep food safe, but pre- and post-harvest points of contamination for fruits and vegetables consumed raw has largely been the responsibility of the food industry. Wildlife and other uncontrollable sources of parasites make treatment of wash water and drinking water essential. Parasites are highly resistant to chlorination and many disinfectants. Cryptosporidium is susceptible to UV, ozone, drying and extreme temperatures. Limited information is available with other parasites, particularly Cyclospora. It should be a priority for the food industry to address pre- and post-harvest points of contamination for fruits and vegetables that are intended to be consumed raw.

A8.7.6 Social sensitivity As a result of high-pro le outbreaks involving fresh produce from developing countries, consumers are concerned about working conditions for food handlers and their access to sanitation facilities. Seafoodborne trematode infections, not yet a major problem, are associated with immigrants from SE Asia; likewise for fascioliasis and hydatidosis there is concern concerning food contamination from immigrant food handlers from Central and South America. Toxoplasmosis and trichinellosis from poorly cooked game meats (bear, wild boar, marine mammals, etc.) are primarily associated with social groups like hunters and native peoples (such as Inuit), who o en consume raw or dried meats. Toxoplasmosis is a recognized concern of physicians for women during pregnancy, but emphasis for prevention is placed on potential contamination from cats rather than from foodborne infection.

A8.6.7 Risk management Risk management is summarized in Table A8.6.3.

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TABLE A8.6.1 Data availability on the burden of disease and food attribution at the regional and global level Global Disease severity/main populations at risk Main food source and attribution Disease in humans Disease severity/ main populations at risk Main food sources

Regional

Parasite species

Disease in humans

Alaria spp.

Yes [1, 5] Rare 3 cases

Anisakis spp.

Blastocystis spp.

Yes [1, 5] Yes [1, 5] Hives and bronchiospasms Raw or undercooked frog in a hunter meat, undercooked wild goose meat Consumers of raw marine Raw marine shes Yes [26–28] 3 cases reported in Canada shes since 1989 Yes [10, 11] Yes 23% of 2896 patients in 48 Associated with irritable bowel syndrome USA states; 2.6% of 216 275 stool specimens Yes Argentina 25% and 43%; Switzerland 16.7-19%; Chile 61.8% Yes Immunocompromised persons, children, elderly, travellers

Yes [12] Associated with irritable bowel syndrome

Yes [13] Well water, tap water, leafy vegetables, food vendors

Cryptosporidium spp. (C. parvum, C. hominis and several other spp.)

Yes [7, 9] Annual domestically acquired foodborne mean cases in USA: 57,616. 90% credible interval: 12,060-166,771

ANNEX 8 REGIONAL REPORTS

Yes [8] 1999-2008 USA: Beverages 50%; Complex foods 50% 3 outbreaks associated with apple cider in US; also green onions, other raw produce, and prepared foods

269

270 Global Disease severity/main populations at risk Yes [8] Immunocompromised persons, travellers Yes [8, 9 1999–2008 USA: Complex foods 21.4%; Produce 78.6% Imported fresh raspberries, mesclun lettuce, basil Main food source and attribution Disease in humans Disease severity/ main populations at risk Main food sources Yes, Consumers of raw freshwater and anadromous shes Yes, Raw freshwater and anadromous shes Residents of Arctic Canada; close association with dogs No data, Contamination of foods with eggs from faeces of dogs, wolves, coyotes

Regional

Parasite species

Disease in humans

Cyclospora cayetanensis

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Diphyllobothrium spp. [14–16] (D. dendriticum, D. latum, D. ursi, D. nihonkaiense)

Echinococcus granulosus [17]

Yes [7, 9] Annual domestically acquired foodborne mean cases in USA: 11 407 (90% credible interval: 137 – 37 673) Foodborne outbreaks in North America yearly since 1995 (spring/summer) Yes Up to 80% prevalence of D. dendriticum in some Inuit communities in Canada. Case of infection with D. ursi reported in British Columbia, Canada in 1973 One case of infection with D. nihonkaiense in Canada No data Number of cases speci cally associated with consumption of contaminated foods is unknown

Regional Disease severity/main populations at risk No data, Contamination of foods with eggs from faeces of dogs, cats, foxes, coyotes Main food source and attribution Disease in humans Disease severity/ main populations at risk Main food sources

Global

Parasite species

Disease in humans

Echinococcus multilocularis [17]

Echinostomidae Yes [1, 2] Raw frogs, sh, snakes, clams snails

Residents of Arctic Canada and Alaska, as well as Canadian prairie provinces and 13 American states; close association with dogs Yes [1, 2] Mostly tourists from Kenya and Tanzania.

Fasciola hepatica

No data, Number of cases speci cally associated with consumption of contaminated foods is unknown Yes [1, 2] 23 cases Several cases reported in Canada (Ontario and Alberta) Yes [1] 1934-2008: 23 cases reported in the USA Yes [1] Liver and bile ducts. Endemic in the USA in lymnaeid snails and herbivores. Most cases imported from a wide geographic range; only 4 locally acquired. Yes [8, 9 Outbreaks in USA attributed to prepared foods and fresh produce Yes [1, 4] Yes Tainted aquatic vegetation (especially watercress) and water Yes [4]

Yes [4] watercress

Giardia duodenalis (syn. G. intestinalis, G. lamblia)

Yes [7] Annual domestically acquired foodborne mean cases in USA: 76 840 (90% credible interval: 51 148 – 109 739)

CHAPTER 1 INTRODUCTION

271

272 Global Disease severity/main populations at risk Yes [1, 2] One USA case from sushi prepared from shes imported from SE Asia Main food source and attribution Disease in humans Disease severity/ main populations at risk Main food sources Yes [1, 2] Yes [1, 2] Recurrent diarrhoea Fish (sushi) reported in 1 case in the US 1 case report suggested salad contaminated with metacercariae from a cutting surface Yes [1] Yes [1] Abdominal pain, fever, Raw white sucker headache, anorexia, diarrhea, nausea, backache. No data No data Yes [1, 2] Raw salmon, steelhead trout, trout eggs

Regional

Parasite species

Disease in humans

Heterophyes heterophyes

Metagonimus spp.

Yes [1, 2] 43 cases (41 in Hawaii) A few cases reported in recent immigrants to Manitoba and Alberta (Canada) Yes [1, 2] 10 cases 2 cases reported in recent immigrants to Alberta (Canada)

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Metorchis conjunctus

Nanophyetes spp.

Yes [2, 6] Outbreak among a group of Korean nationals who consumed raw white sucker freshly caught in river near Montreal, Canada; 17 of 19 individuals became symptomatic Yes [1, 2] Yes [1, 2] 21 cases, mostly Northwestern US

Regional Disease severity/main populations at risk Yes [1, 2] Raw or under-cooked freshwater sh Yes Main food source and attribution Disease in humans Disease severity/ main populations at risk Yes Main food sources

Global

Parasite species

Disease in humans

Opisthorchis viverrini Yes [1, 2] and Clonorchis ca. 1270 cases 1890–2009, sinensis mostly individual case reports Commonly reported among immigrants from SE Asia to Canada

Yes [1, 2] Freshwater sh, especially cyprinids

Paragonimus spp. P. westermani P. kellicotti P. mexicanus

Yes [1–3] 71 cases reported 1910–2009. P. kellicotti: 7 cases 1968–2008, 14 cases 2009–2010. A few cases reported in immigrants to Canada from Italy, Malaysia, Philippines. One domestic case in Quebec, who sold live snails and crustaceans from exotic food section of department store.

Yes [1, 2] Group 1 carcinogens; liver and bile duct cancer. Infections mainly imported into the USA. Through the 1970s most were imported in Chinese, Japanese and Korean immigrants or Caucasians who had resided in China. Beginning in 1979, SE Asians were a major source of imported cases, especially those from Thai refugee camps. Yes [1, 3] Most cases in 1970s and 1980s imported by SE Asian refugees from Thai camps, immigrants from Korea and Philippines; some co-infections with other helminths. Yes [1, 3] Raw or undercooked cray sh and crabs Yes Yes

Yes

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273

274 Global Disease severity/main populations at risk Consumers of raw marine shes Yes [9] Immunocompromised persons, pregnant women, consumers of raw meat (Inuit people) Raw marine shes Main food source and attribution Disease in humans Disease severity/ main populations at risk Main food sources Yes [8, 9] 1999–2008 USA: domestic meats 69.6%; game 20.4% produce 7.0% dairy 2.4% seafood 0.5% Outbreaks in USA attributed to rare hamburger, rare lamb, raw goat milk. Outbreak in Canada (northern Quebec) involved 4 pregnant Inuit women who had consumed raw or dried seal or caribou meat Yes [23] Commercial swine in Canada are currently Trichinella-free

Regional

Parasite species

Disease in humans

Pseudoterranova spp.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Toxoplasma gondii

Yes [29] 1 case reported in Canada in 1973 Yes [7] Annual domestically acquired foodborne mean cases in USA: 86 686 (90% credible interval: 64–861 – 111 912)

Trichinella spiralis

No data [23] Some of the 43 Trichinella spp. cases may be T. spiralis

Regional Disease severity/main populations at risk Yes [24, 25] Inuit and aboriginal people, hunters Yes Yes [18] 431 Yes [18] Black bear raw meat Yes [24, 25] Black bear meat, grizzly bear meat, walruses Main food source and attribution Disease in humans Disease severity/ main populations at risk

Global Main food sources

Parasite species

Disease in humans

Trichinella nativa

Trichinella murrelli

Yes [18] Horse meat

Trichinella pseudospiralis Trichinella spp. [23] Yes [18–23] Inuit and aboriginal people, hunters Yes [18–23] Of the 72 cases, 31 eat wild game (31), bear (29), cougar (1),wild boar (1) and pork(12) meat. Of the 66 cases, bear, deer, walrus, seal pork, and beef meat

ANNEX 8 REGIONAL REPORTS

Trichinella genotype T6

Yes [24, 25] 95 cases reported between 1982-2009 in Northern Canada Yes [18] In 2008, 30 of 38 attendees of an event US. No reported cases in Canada No reported cases in Canada Yes [18–23] 1997–2001: 72 cases reported. 2002–2007: 66 cases reported. 2008: 5 more cases 43 cases reported in Canada in 1999 No reported cases in Canada

275

Reference cited in Table A8.6.1 01. 02. Fried, B. & Abruzzi, A. 2010. Foodborne trematode infections of humans in the United States of America. Parasitology Research. 106(6): 1263–1280. Dixon, B.R. & Flohr, R.B. 1997. Fish- and shell sh-borne trematode infections in Canada. In: Proceedings of the 2nd Seminar on Foodborne Parasitic Zoonoses: Current Problems, Epidemiology, Food Safety and Control. Khon Kaen, Thailand, 6–9 Dec. 1995. Southeast Asian Journal of Tropical Medicine and Public Health, 28(Suppl. 1): 58–64. Lane, M.A., Marcos, L.A., Onen, N.F., Demertzis, L.M., Hayes, E.V., Davila, S.Z., Nurutdinova, D.R., Bailey, T.C. & Weil, G.J. 2012. Paragonimus kellicotti uke Infections in Missouri, USA. Emerging Infectious Diseases, 18(8): 1263–1267. Keiser, J. & Utzinger, J. 2009. Foodborne trematodiases. Clinical Microbiology Reviews, 22(3): 466–483. Kramer, M.H., Eberhard, M.L. & Blankenberg, T.A.1996. Respiratory symptoms and subcutaneous granuloma caused by mesocercariae: a case report. American Journal of Tropical Medicine and Hygiene, 55(4): 447–148. MacLean, J.D., Arthur, J.R., Ward, B.J., Gyorkos, T.W., Curtis, M.A. & Kokoskin, E. 1996. Common-source outbreak of acute infection due to the North American liver uke Metorchis conjunctus. Lancet, 347(8995): 154–158. Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., Jones, J.L. & Gri n, P.M. 2011. Foodborne illness acquired in the United States – major pathogens. Emerging Infectious Diseases, 17(1): 7–15. Batz, M.B., Ho mann, S.M. & Glenn, J.G. Jr. 2012. Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. Journal of Food Protection, 75(7): 1278–1291. Dixon, B.R., Fayer, R., Santin, M., Hill, D.E. & Dubey J.P. 2011. Protozoan parasites: Cryptosporidium, Giardia, Cyclospora, and Toxoplasma. pp. 349–370 (Chapter 24), in: J. Hoorfar (editor). Rapid Detection, Characterization and Enumeration of Foodborne Pathogens. ASM Press, Washington DC, USA. Amin, O.M. 2002. Seasonal prevalence of intestinal parasites in the United States during 2000. American Journal of Tropical Medicine and Hygiene, 66(6): 799–803. Kappus, K.K., Juranek, D.D. & Roberts, J.M. 1991. Results of testing for intestinal parasites by state diagnostic laboratories, United States, 1987. Morbidity and Mortality Weekly Report, CDC Surveillance Summaries, 40: 25–245. Jimenez-Gonzalez, D.E., Martinez-Flores, W.A., Reyes-Gordillo, J. and 9 others. 2012. Blastocystis infection is associated with irritable bowel syndrome in a Mexican patient population. Parasitology Research, 110(3): 1269–1275. Tan, K.S.W. 2008. New Insights on classi cation, identi cation and clinical relevance of Blastocystis spp. Clinical Microbiology Reviews, 21: 639–665. Gyorkos, T.W., MacLean, J.D. Serhir, B. & Ward, B. 2003: Prevalence of parasites in Canada and Alaska: Epidemiology past and present. pp. 77–88, in: H. Aku o, E. Linder, I. Ljungström and M. Wahlgren (editors). Parasites of the Colder Climates. Taylor and Francis. New York, NY, USA. Margolis, L., Rausch, R.L. & Robertson, E. 1973. Diphyllobothrium ursi from man in British Columbia-- rst report of this tapeworm in Canada. Canadian Journal of Public Health, 64(6): 588–589. Wicht ,B,, Scholz, T., Peduzzi, R. & Kuchta, R. 2008. First record of human infection with the tapeworm Diphyllobothrium nihonkaiense in North America. American Journal of Tropical Medicine and Hygiene, 78(2): 235–238. Jenkins, E.J., Schurer, J.M. & Gesy, K.M. 2011. Old problems on a new playing eld: helminth zoonoses transmitted among dogs, wildlife, and people in a changing northern climate. Veterinary Parasitology, 182(1): 54–69. Hall, R.L., Lindsay, A., Hammond, C. and 13 others. 2012. Outbreak of human trichinellosis in northern California caused by Trichinella murrelli. American Journal of Tropical Medicine and Hygiene, 87(2): 297–302.

03.

04. 05.

06.

07.

08.

09.

10. 11.

12.

13. 14.

15.

16.

17.

18.

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19. 20.

Roy, S.L., Lopez, A.S. & Schantz, P.M. 2003. Trichinellosis surveillance – United States, 1997– 2001. Morbidity and Mortality Weekly Report, CDC Surveillance Summaries, 52(6): 1–8. Kennedy, E.D., Hall, R.L., Montgomery, S.P., Pyburn, D.G., Jones, J.L. & Centers for Disease Control and Prevention. 2009. Trichinellosis surveillance - United States, 2002– 2007. Morbidity and Mortality Weekly Report, CDC Surveillance Summaries, 58(9): 1–7. Anon. Various dates. National Noti able Diseases Database, Public Health Agency of Canada. Appleyard, G.D. & Gajadhar, A.A. 2000. A review of trichinellosis in people and wildlife in Canada. Canadian Journal of Public Health-Revue Canadienne de Sante Publique, 91(4): 293–297. Gajadhar, A.A., Bisaillon, J.R. & Appleyard, G.D. 1997. Status of Trichinella spiralis in domestic swine and wild boar in Canada. Canadian Journal of Veterinary Research-Revue Canadienne de Recherche Veterinaire, 61(4): 256–259. Proulx, Jean-François. 2011. Department of Public Health, Nunavik Regional Board of Health and Social Services. Pers. comm. in response to request for data. Forbes, Lorry. 2011. Centre for Foodborne and Animal Parasitology, Canadian Food Inspection Agency. Pers. comm. in response to request for data. Kowalewska-Grochowska, K., Quinn, J., Perry, I. & Sherbaniuk, R. 1989. A case of anisakiasis – Alberta. Canadian Disease Weekly Reports, 15(44): 221–223. Couture, C., Measures, L., Gagnon, J. & Desbiens, C. 2003. Human intestinal anisakiosis due to consumption of raw salmon. American Journal of Surgical Pathology, 27(8): 1167–1172. Bhat, M. & Cleland, P. 2010. Gastric anisakiasis. Clinical Gastroenterology and Hepatology, 8(8): A20. Kates, S., Wright, K.A. & Wright, R. 1973. A case of human infection with the cod nematode Phocanema sp. American Journal of Tropical Medicine and Hygiene, 22(5): 606–608.

21. 22.

23.

24, 25. 26. 27. 28. 29.

TABLE A8.6.2 Data availability for parasite prevalence or concentration in the main food categories Alaria spp. Seafood Anisakis spp. Seafood Yes [13–15] Marine sh, squid. Blastocystis spp. Vegetables Other Yes [9] Leafy vegetables. Water. Yes [1] Frogs.

Cryptosporidium spp. [7] Dairy Seafood Fruits Vegetables Other Yes [8] Un-pasteurized milk. Molluscan shell sh. Yes. Apple cider. Yes. Green onions; produce. Water; prepared foods.

Cyclospora spp. [7] Fruits Vegetables Other Yes. Raspberry. Yes. Lettuce, basil, snow peas, watercress. Water.

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277

Diphyllobothrium spp. Seafood Yes [10–12] Raw freshwater and anadromous sh. Echinostomidae Seafood Yes [1. 2] Frogs, snakes, sh, clams, snails. Fasciola hepatica Vegetables Giardia spp. [7] Seafood Vegetables Other Molluscan shell sh. Yes; fresh produce. Water; prepared foods. Yes [1] Aquatic vegetation: watercress.

Heterophyes heterophyes Seafood Yes [2] Sushi prepared from sh imported from SE Asia. Metagonimus spp. Seafood Yes [2] Sushi; possibly salad contaminated with metacercariae. Nanophyetes spp. Seafood Yes [1, 2] Raw salmon, steelhead trout, trout eggs. Opisthorchis viverrini and Clonorchis sinensis Seafood Yes [1. 2] Numerous species of freshwater sh. Paragonimus kellicotti Seafood Yes [3] Freshwater crustaceans (100%). Paragonimus mexicanus Seafood Freshwater crustaceans (100%). Paragonimus westermani Seafood Yes [1. 2] Freshwater crustaceans (100%): cray sh, crabs. Pseudoterranova spp. Seafood Yes [16] Marine sh. Trichinella spp. [4–6] Pork Game Yes. Pork meat Yes. Bear, walrus, wild boar, cougar.

Toxoplasma spp. [7] Beef Dairy Pork Poultry Game Seafood Yes Yes Yes Yes Yes; caribou, seal Molluscan shell sh

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Fruits Vegetables Other

No data, but oocyst contamination is feasible No data, but oocyst contamination is feasible Water

Trypanosoma cruzi Very little substantive data available. References cited in Table A8.6.2 01. 02. Fried, B. & Abruzzi, A. 2010. Foodborne trematode infections of humans in the United States of America. Parasitology Research. 106(6): 1263–1280. Dixon, B.R. & Flohr, R.B. 1997. Fish- and shell sh-borne trematode infections in Canada. In: Proceedings of the 2nd Seminar on Foodborne Parasitic Zoonoses: Current Problems, Epidemiology, Food Safety and Control. Khon Kaen, Thailand, 6–9 Dec. 1995. Southeast Asian Journal of Tropical Medicine and Public Health, 28(Suppl. 1): 58–64. Lane, M.A., Marcos, L.A., Onen, N.F., Demertzis, L.M., Hayes, E.V., Davila, S.Z., Nurutdinova, D.R., Bailey, T.C. & Weil, G.J. 2012. Paragonimus kellicotti uke Infections in Missouri, USA. Emerging Infectious Diseases, 18(8): 1263–1267. Appleyard, G.D. & Gajadhar, A.A. 2000. A review of trichinellosis in people and wildlife in Canada. Canadian Journal of Public Health-Revue Canadienne de Sante Publique, 91(4): 293–297. Kennedy, E.D., Hall, R.L., Montgomery, S.P., Pyburn, D.G., Jones, J.L. & Centers for Disease Control and Prevention. 2009. Trichinellosis surveillance - United States, 2002– 2007. Morbidity and Mortality Weekly Report, CDC Surveillance Summaries, 58(9): 1–7. Roy, S.L., Lopez, A.S. & Schantz, P.M. 2003. Trichinellosis surveillance – United States, 1997–2001. Morbidity and Mortality Weekly Report, CDC Surveillance Summaries, 52(6): 1–8. Dixon, B.R., Fayer, R., Santin, M., Hill, D.E. & Dubey J.P. 2011. Protozoan parasites: Cryptosporidium, Giardia, Cyclospora, and Toxoplasma. pp. 349–370 (Chapter 24), in: J. Hoorfar (editor). Rapid Detection, Characterization and Enumeration of Foodborne Pathogens. ASM Press, Washington DC, USA. Harper, C.M., Cowell, N.A., Adams, B.C., Langley, A.J. & Wohlsen, T.D. 2002. Outbreak of Cryptosporidium linked to drinking unpasteurised milk. Communicable Diseases Intelligence Quarterly Report, 26(3): 449–450. Leber, A.L. 1999. Intestinal amebae. Clinical Laboratory Medicine, 19(3): 601–619, vii. [Review]. Gyorkos, T.W., J.D. MacLean, B. Serhir & Ward, B. 2003: Prevalence of parasites in Canada and Alaska: Epidemiology past and present. pp. 77–88, in: H. Aku o, E. Linder, I. Ljungström and M. Wahlgren (editors). Parasites of the Colder Climates. Taylor and Francis. New York, NY, USA. Margolis, L., Rausch, R.L. & Robertson, E. 1973. Diphyllobothrium ursi from man in British Columbia-- rst report of this tapeworm in Canada. Canadian Journal of Public Health, 64(6): 588–589. Wicht ,B,, Scholz, T., Peduzzi, R. & Kuchta, R. 2008. First record of human infection with the tapeworm Diphyllobothrium nihonkaiense in North America. American Journal of Tropical Medicine and Hygiene, 78(2): 235–238. Kowalewska-Grochowska, K., Quinn, J., Perry, I. & Sherbaniuk, R. 1989. A case of anisakiasis – Alberta. Canadian Disease Weekly Reports, 15(44): 221–223. Couture, C., Measures, L., Gagnon, J. & Desbiens, C. 2003. Human intestinal anisakiosis due to consumption of raw salmon. American Journal of Surgical Pathology, 27(8): 1167–1172. Bhat, M. & Cleland, P. 2010. Gastric anisakiasis. Clinical Gastroenterology and Hepatology, 8(8): A20. Kates, S., Wright, K.A. & Wright, R. 1973. A case of human infection with the cod nematode Phocanema sp. American Journal of Tropical Medicine and Hygiene, 22(5): 606–608.

03.

05.

06.

07.

08.

09. 10.

11.

12.

13. 14. 15. 16.

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279

TABLE A8.6.3 Data availability for risk management options in North America for each parasite-commodity combination NOTE: The authors were asked to consider all combinations of the particular parasite and the main food categories, namely Beef, Dairy, Pork, Poultry, Game, Seafood, Fruit, Vegetables and Other.

Alaria spp. [1] Seafood R Anisakis spp., Pseudoterranova spp. Seafood Yes [3] Fish surveillance studies; candling of llets at processing plants; use of pre-frozen sh for sushi; consumer education

Blastocystis spp. Fruit Good agricultural practices, e.g., water quality, worker hygiene, compost requirements; consumer and food handler education regarding fresh produce Good agricultural practices; consumer and food handler education regarding fresh produce

Vegetables

Cryptosporidium spp. Beef Dairy Seafood Fruit Yes [1] Heat and freezing Yes [1] Pasteurization Yes [5] Shell sh sanitation programs Yes [5] Good agricultural practices, e.g., water quality, worker hygiene, compost requirements; consumer and food handler education regarding fresh produce; surveillance studies; disinfectants Yes [5] Good agricultural practices; consumer and food handler education regarding fresh produce; surveillance studies; disinfectants Yes [1] Fruit juice pasteurization

Vegetables Other

Cyclospora cayetanensis Fruit Vegetables Yes [5] Good agricultural practices; import restrictions; surveillance studies; former “Model Plan of Excellence” program in Guatemala; disinfectants Yes [5] Good agricultural practices; import restrictions; surveillance studies; disinfectants

Diphyllobothrium spp. Seafood Trichinella spp. Pork Game Routine surveillance of commercial swine Surveillance of wildlife harvested for food; trichinellosis program in Arctic Canada (walrus testing); hunter education Yes [5] Fish surveillance studies; wild-caught vs aquaculture (pelleted feed); consumer education

Echinostomidae, Heterophyes heterophyes Seafood Yes [1–3] Consumer education (cooking/freezing); good sanitation; import restrictions

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Fasciola hepatica [1] Vegetables Other R R

Giardia duodenalis (syn. G. lamblia, G. intestinalis) Seafood Fruit Vegetables Yes [5] Shell sh sanitation programmes Yes [5] Good agricultural practices; surveillance studies Yes [5] Good agricultural practices; surveillance studies

Metagonimus spp. Seafood Yes [2, 3] Consumer education (cooking/freezing); good sanitation; import restrictions

Nanophyetes spp. Seafood Yes [1–3] Consumer education (cooking/freezing); good sanitation; import restrictions

Opisthorchis viverrini, Clonorchis sinensis and Paragonimus westermani Seafood Yes [1–3] Consumer education (cooking/freezing); good sanitation; import restrictions Paragonimus kellicotti Seafood Yes [6] Consumer education: avoid eating raw cray sh Paragonimus mexicanus Seafood R Toxoplasma gondii Beef Dairy Pork Poultry Game Seafood Yes [5, 6] Meat surveillance studies; consumer and food handler education (cooking and freezing) Yes [5, 6] Milk pasteurization requirements Yes [5, 6] Meat surveillance studies; consumer and food handler education (cooking and freezing) Yes [5, 6] Meat surveillance studies; consumer and food handler education (cooking and freezing) Yes [5, 6] Meat surveillance studies; seroprevalence studies on wildlife; consumer and food handler education (cooking and freezing) Yes [5, 6] Shell sh sanitation programs

References cited in Table A8.6.3 1. 2. Fried, B. & Abruzzi, A. 2010. Foodborne trematode infections of humans in the United States of America. Parasitology Research. 106(6): 1263–1280. Dixon, B.R. & Flohr, R.B. 1997. Fish- and shell sh-borne trematode infections in Canada. In: Proceedings of the 2nd Seminar on Foodborne Parasitic Zoonoses: Current Problems, Epidemiology, Food Safety and Control. Khon Kaen, Thailand, 6–9 Dec. 1995. Southeast Asian Journal of Tropical Medicine and Public Health, 28(Suppl. 1): 58–64. Adams, A.M., Murrell, K.D. & Cross, J.H. 1997. Parasites of sh and risks to public health. Revue technique et scienti que OIE, 16(2): 652–660.

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281

4. 5.

Robertson, L.J. & Fayer, R. 2012. Cryptosporidium spp. pp. 33–64, in: L.J. Robertson and H.V. Smith (editors). Foodborne Protozoan Parasites. Nova Science Publishers. Dixon, B.R., Fayer, R., Santin, M., Hill, D.E. & Dubey J.P. 2011. Protozoan parasites: Cryptosporidium, Giardia, Cyclospora, and Toxoplasma. pp. 349–370 (Chapter 24), in: J. Hoorfar (editor). Rapid Detection, Characterization and Enumeration of Foodborne Pathogens. ASM Press, Washington DC, USA. Lane, M.A., Marcos, L.A., Onen, N.F., Demertzis, L.M., Hayes, E.V., Davila, S.Z., Nurutdinova, D.R., Bailey, T.C. & Weil, G.J. 2012. Paragonimus kellicotti uke Infections in Missouri, USA. Emerging Infectious Diseases, 18(8): 1263–1267. Lindsay, D.S., Dubey, J.P., Santin, M. & Fayer, R. 2012. Coccidia and other protozoa. pp. 895907 (Chapter 66), in: J.J. Zimmerman, L.A. Karriker, A. Ramirez, K.J. Schwartz and G.W. Stevenson (editors). Diseases of Swine. 10th Edition. Wiley-Blackwell, Ames, Iowa, USA.

TABLE A8.6.4 Data availability for Central America Disease severity/ Main food source and main attribution populations at risk

Parasite species

Disease in humans

Alaria spp. Anisakis spp. Blastocystis spp. Yes [8, 9] 30% of 456 children in day care centres in Cuba; 39% of local populations in Cuba Yes [1–5] Endemic in Guatemala (2.3% prevalence). Among 182 raspberry farm workers and family members examined in Guatemala, 3.3% had Cyclospora infection; Another study failed to detect oocysts among raspberry farm workers in Guatemala

Cyclospora cayetanensis

Yes [6, 16] Outbreak in Quebec, Canada, in 2005 associated with fresh basil from Mexico. Reported in lettuce from local markets in Costa Rica

Cryptosporidium spp. Diphyllobothrium spp. (D. dendriticum, D. latum, D. ursi, D. nihonkaiense)

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Parasite species

Disease in humans

Disease severity/ Main food source and main attribution populations at risk

Echinococcus granulosus, E. multilocularis Echinostomidae Entamoeba histolytica Yes [11] In Mexico, Entamoeba histolytica antibodies found in 4.49% Yes [7–9] Nail biting and eating unwashed vegetables raw were signi cantly associated with infection in hospitalized children in Cuba; 54.6% of 456 children in day cares in Cuba; 25% of local populations in Cuba.

Fasciola hepatica Giardia duodenalis (syn. G. intestinalis, G. lamblia)

Heterophyes heterophyes Metagonimus spp. Nanophyetes spp. Opisthorchis viverrini and Clonorchis sinensis Paragonimus spp. Pseudoterranova spp. Taenia solium Yes [12–15] 4.9–10.8% tested positive for cysticercosis in villages in Mexico; T. solium taeniasis and cysticercosis are endemic in Guatemala; Clinical incidence of neurocysticercosis can reach 7% in Mexico. Honduras: cysticercosis annual incidence ca. 30.

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283

Parasite species

Disease in humans

Disease severity/ Main food source and main attribution populations at risk

Toxoplasma gondii

Yes [10] Estimated incidence in Honduras 36 000/yr

Trichinella spp. References cited in Table A8.6.4 01. 02. 03. Cama, V. 2006. Coccidian parasites. pp. 33–55, in: Y.R. Ortega (editor). Foodborne Parasites. Springer, New York, NY, USA. Ortega, Y.R. & Sanchez, R. 2010. Update on Cyclospora cayetanensis, a foodborne and waterborne parasite. Clinical Microbiology Reviews, 23(1): 218–234. Bern, C., Hernandez, B., Lopez, M.B., Arrowood, M.J., de Mejia, M.A., de Merida, A.M., Hightower, A.W., Venczel, L., Herwaldt, B.L. & Klein. R.E. 1999. Epidemiologic studies of Cyclospora cayetanensis in Guatemala. Emerging Infectious Diseases, 5: 766–774. Bern, C., Hernandez, B., Lopez, M.B., Arrowood, M.J., De Merida, A.M. & Klein, R.E. 2000. The contrasting epidemiology of Cyclospora and Cryptosporidium among outpatients in Guatemala. American Journal of Tropical Medicine and Hygiene, 63(56): 231–235. Pratdesaba, R.A., González, M., Piedrasanta, E., Mérida, C., Contreras, Vela, C., Culajay, F., Flores, L. & Torres, O. 2001. Cyclospora cayetanensis in three populations at risk in Guatemala. Journal of Clinical Microbiology, 39: 2951–2953. Calvo, M., Carazo, M., Arias, M.L., Chaves, C., Monge, R. & Chinchilla, M. 2004. [Prevalence of Cyclospora spp., Cryptosporidium spp., microsporidia and fecal coliform determination in fresh fruit and vegetables consumed in Costa Rica.] [In Spanish] Archivos Latinamericos de Nutricion, 54(4): 428–432. Bello, J., Núñez, F.A., González, O.M., Fernández, R., Almirall, P. & Escobedo, A.A. 2011. Risk factors for Giardia infection among hospitalized children in Cuba. Annals of Tropical Medicine and Parasitology, 105(1): 57–64. Mendoza, D., Núñez, F.A., Escobedo, A., Pelayo, L., Fernández, M., Torres, D. & Cordoví, R.A. 2001. [Intestinal parasitic infections in 4 child day-care centers located in San Miguel del Padrón municipality, Havana City, 1998]. [Article in Spanish] Revista Cubana de Medicina Tropical, 53(3): 189–193. Escobedo, A.A., Cañete, R. & Núñez, F.A. 2007. Intestinal protozoan and helminth infections in the Municipality San Juan y Martínez, Pinar del Río, Cuba. Tropical Doctor, 37(4): 236–238. Dominguez, W. 2009. Estudio de caso – Enfermedades Transmitidas por alimetos en Honduras. pp. 139–157, in: Enfermedades transmitidas por alimentos y su impacto socioeconómico. Estudios de caso en Costa Rica, El Salvador, Guatemala, Honduras y Nicaragua. [FAO] Informe Técnico Sobre Ingeniería Agrícola Y Alimentaria. No.6. See: www. fao.org/docrep/011/i0480s/i0480s00.htm Gonzalez, C.R., Isibasi, A., Ortiznavarrette, V., Paniagua, J., Garcia, J.A., Ramirez, A., Salvatierra, B., Tapia, R., Sepulveda, J., Gutierrez, G. & Kumate, J. 1995. Prevalence of antibodies against Entamoeba histolytica in Mexico measured by ELISA. Epidemiology and Infection, 115(3): 535–543. Sarti, E., Schantz, P. M., Plancarte, A., Wilson, M., Gutierrez, I. O., Lopez, A.S., Roberts, J. & Flisser, A. 1992. Prevalence and risk factors for Taenia solium Taeniasis and cysticercosis in humans and pigs in a village in Morelos, Mexico. American Journal of Tropical Medicine and Hygiene, 46: 677–685.

04.

05.

06.

07.

08.

09.

10.

11.

12.

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13.

Sarti, E., Schantz, P.M., Plancarte, A., Wilson, M., Gutierrez, I., Aguilera, J., Roberts, J. & Flisser, A. 1994. Epidemiological investigation of Taenia solium Taeniasis and cysticercosis in a rural village of Michoacan State, Mexico. Transactions of the Royal Society of Tropical Medicine and Hygiene, 88: 49–52. Garcia-Noval, J., Allan, J.C., Fletes, C., Moreno, E., Demata, F., Torresalvarez, R., Dealfaro, H.S., Yurrita, P., Higuerosmorales, H., Mencos, F. & Craig, P.S. 1996. Epidemiology of Taenia solium Taeniasis and cysticercosis in two rural Guatemalan communities. American Journal of Tropical Medicine and Hygiene, 55: 282–289. Flisser, A. 1988. Neurocysticercosis in Mexico. Parasitology Today, 4: 131–137. Milord, F., Lampron-Goulet, E., St-Amour, M., Levac, E. & Ramsay, D. 2012. Cyclospora cayetanensis: a description of clinical aspects of an outbreak in Quebec, Canada. Epidemiology and Infection, 140(4): 626–632.

14.

15. 16.

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285

ANNEX 8.7 SOUTH AMERICA A8.7.1 Report preparation e Group members were: Jorge Enrique Bolpe, Argentina, and Jorge Enrique Gómez-Marín, Colombia. eir sources included systematic literature reviews, involving bibliographic database searches (Pubmed, Scopus, Scielo) and own data from unpublished reports (Dr Gómez-Marin). Additionally, literature reviews of bulletins, national reports, book articles and technical guidelines were used (Dr Bolpe).

A8.7.2 Data availability in humans and food attribution Good evidence exists about Toxoplasma presence in meat for human consumption, although some countries have only limited data. Good quality reports exist of foodborne Trypanosoma infection. ere is good information on the quantity and quality of regional data concerning trichinellosis and cystic echinococcosis in humans in Argentina and other countries in southern of South America, probably because these diseases are included in the national epidemiological surveillance systems in the a ected countries. ere is also valuable information regarding the identi cation of food infected with Trichinella, with the identi cation of the speci c species (T. spiralis). Data on the burden of disease and food attribution are summarized in Table A8.7.1, and data on parasite prevalence, incidence and concentration in the main food categories are covered in Table A8.7.2.

A8.7.3 Agri-food trade All the countries in South America export fruits to many continents. Notably, during the last decade, Colombian fruit exports doubled to a total US$ 800 million and more than 1800 ton (Proexport data). Brazil and Argentina export signi cant volumes of horse and beef meat, while pork meat exportation is less important. At present there are no data indicating the presence of parasites in horses. However, in Argentina, because of trichinellosis endemicity, all horse and pork meat for exportation must be certi ed with a negative test of peptic digestion performed by the National Animal Health Service.

A8.7.4 Consumer perception e recent free-trade agreement with the United States of America has raised important questions concerning sanitary security. In Colombia, for example, wide public consumer debates have developed regarding the origin and security of chicken imports from United States of America. A recent urban outbreak of foodborne trypanosomiasis in a school in Caracas, Venezuela, portends a new epidemiological situation for this disease in Brazil, Colombia and Venezuela. For trichi-

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nellosis consumer perception in Argentina, some parts of the population show a consumer willingness to accept risk in food consumption without sanitary control. In Argentina, many people are regular consumers of pork in the form of stu ed products, such as sausages produced by local butchers, and avoid foods processed under industrial conditions with sanitary control. is is enhanced by current cultural trends. In many family outbreaks, the consumers who have bred pigs using poor husbandry produced food without the detection of Trichinella infection in pig carcasses. Cystic echinococcosis from the ingestion of green vegetables contaminated with oncospheres is possible in rural areas the parasite is endemic, where cultural practice encourage the parasitic cycle through the slaughter of domestic sheep and the feeding of dogs with raw viscera.

A8.7.5 Social sensitivity ere have been increased foodborne outbreaks in most of countries in the region, re ecting cultural changes and increases in the frequency of eating outside the home. eses outbreaks have been widely publicized, and public pressure developed to reinforce health authority controls. Trichinellosis e economic impact of trichinellosis is apparent in the control system for detecting this infection in potential Trichinella carriers, mainly in slaughterhouses, and the occurrence of the disease in human and animals. e economic loss due to the destruction of infected carcases is a signi cant economic loss in Argentina. e cost for human treatment has been estimated at US$ 6000 in the United Staes of America, and at US$ 3000 in Europe. Cystic echinococcosis In a Regional Socio-economic Impact of Cystic Echinococcosis (CE) in Argentina, Brazil, Chile and Uruguay, DALYs calculated for the region as a measure of damage caused by CE were 1551.83 due to premature death and 1766.93 due to di erent degrees of disability, both values adjusted for reported cases. e overall monetary cost of CE in the countries—collating human cases, the lost income due to relapse and morbidity, and livestock losses associated with the condemnation of the liver, reduced carcass weight, loss of milk production, decreased fertility and wool yield—was estimated in the range of at least US$ 75 million to a maximum of US$ 97 million (See ref. [83] in Table A8.7.1). For Global Socio-economic Impact, when no underreporting is assumed, the estimated human burden of disease is 285 407 DALYs or an annual loss of US$ 193 530 000.

A8.7.6 Risk management Data are summarized in Table A8.7.3. ANNEX 8 REGIONAL REPORTS

287

288 Global level Disease severity/ main population at risk Disease in humans Yes [77] Yes [78] Low prevalence Yes, but no data reported Main food source and attribution Disease severity/main population at risk Main food sources and attributions Yes [77] Pigs Yes [53] Low prevalence; infrequent cases of diarrhoea Yes [33, 34] Uncon rmed, some genotypes. Pre-school children, some adults with irritable bowel syndrome Yes [36] Eggs, plants Yes [37] Blastocystis has a worldwide distribution and is o en the most commonly isolated organism in parasitological surveys (up to 50% in some cohorts). Extrapolating from available prevalence data, the parasite colonizes the intestine of more than 1 ×109 people worldwide Yes [50] Yes [49] Raspberry, plants (lettuce) Yes [38–40] Uncon rmed, some genotypes associated to diarrhoea, some studies indicates association with irritable bowel syndrome Yes [39, 41, 42] Plants, food handlers, pigs, chicken Yes [48] Outbreaks diarrhoeal disease Yes [51] Yes [49]

TABLE A8.7.1 Data availability on the burden of disease and food attribution for South America at the regional and global levels

Regional level

Species

Disease in humans

Balantidium coli

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Blastocystis spp.

Yes [53, 76] Low prevalence: Bolivia 1–5.5%; Colombia 1.8% Yes [29–32, 43] 36–49% in Colombia in pre-school children; 16%–38% Venezuela; 22% Argentina; 26% Parana, Brazil; 57% Mapuera community, Brazil; 41.3–62.3% Chile. B. hominis Argentina: B. Aires Province – prevalence in 119 children age 1 to 14 years old (urban: 26.9%; peri-urban: 46.2%; rural: 31.7%)

Cyclospora cayetanensis

Yes [44–47] 18–6% Perú; 2% Guatemala 11.9% Venezuela

Regional level Disease severity/ main population at risk Yes [12, 79–85] 3.8 ×106 rural inhabitants live in risk area. Disease in humans Yes [12, 79–85] The most conservative estimate of global DALYs lost is 285,407, with no consideration for disease underreporting. Yes [12, 79–85] Ingestion of vegetables or polluted water with infected canine faeces. Main food source and attribution Disease severity/main population at risk Main food sources and attributions

Global level

Species

Disease in humans

ANNEX 8 REGIONAL REPORTS

Echinococcus Yes [12, 79–85] granulosus Over 2000 new human cases are reported every year in the region of South America. Incidence from 41 per 100 000 in the Patagonian region in southern Argentina, 80 per 100 000 in the XI Region of Chile; up to 100 per 100 000 in the Flores Department of Uruguay. Infection rates of 5.5% in 1986 in Black River, Argentina; 14.2% in 1988 in Loncopué, Neuquén, Tacuarembo, Uruguay; 1.6% in 1997 in Florida, Uruguay; 3.6% in 1998 in Peach, Uruguay; 5.1% in 1999 in Vichaycocha, Peru. 1418 cases have also been reported by ultrasound screening on asymptomatic human population. Argentina: Morbidity in 1987–1996: 5248 human cases, 1997–2005: 4079 human cases Argentina: between 2006 and 2010 1883 suspected Hydatidosis cases were reported. Argentina, Brazil, Chile and Uruguay: DALYs 1551.83 to 1766.93 adjusted for reported cases. Chile: 2004 estimates an incidence of 10 per 100 000, with mortality 0.3–0.4 per 100 000. Brazil: see [85] for data on Rio Grande do Sul

289

290 Global level Disease severity/ main population at risk Disease in humans Yes [72] Yes [73] Yes [71] Low prevalence when studies di erentiated pathogenic from non-pathogenic. Yes, but no data reported. Main food source and attribution Disease severity/main population at risk Main food sources and attributions Yes [74, 75] but little data Only one report di erentiated pathogenic from non-pathogenic. Only E. dispar was found in food handlers Yes [1–3, 86] Case spread, by gender, province, diagnostic method, treatment, etc. Yes [1–3, 86] Ingestion of freshwater plants carrying infective metacercaria, watercress Yes [55,56] Yes [57] In developing countries around 20% (4–43%) and in developed countries 5% (3–7%) Yes [54] Yes [56] Canned salmon, sandwiches, noodle salad, fruit salad, raw vegetables, ice

Regional level

Species

Disease in humans

Entamoeba histolytica

Yes [69, 70] Colombia: 0.6–1.4%

Fasciola hepatica

Yes [1–3, 86] Argentina – 619 autochthonous cases from 13 Provinces, in 58 reports of di erent kinds analysed up to 2010.

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Giardia spp.

Yes [54] Yes [34, 43, 52, 53] Mexico 50%; Colombia 15,0% Retard in cognition Argentina: prevalence of Giardia development duodenalis (syn. G. lamblia, G. intestinalis) in 119 children age 1 to 14 years old – urban 9.6%; peri-urban 34.6%; rural 7.3% Argentina: in multicentre studies using data from di erent provinces – prevalence of Giardia duodenalis (syn. G. lamblia, G. intestinalis) (13.17%) in 1 to 3 year-old children in the country 2004–05.

Regional level Disease severity/ main population at risk Disease in humans Yes [62] Low prevalences Yes [34, 61] No, rare cases of diarrhoea Low prevalence. Not reported Main food source and attribution Disease severity/main population at risk

Global level Main food sources and attributions Yes [66–68] Food handlers

Species

Disease in humans

Hymenolepis nana

Yes [59–61] Children: 1%-6.6% Peru; 1% -14% Venezuela: 31% in aborigines in Salta in Argentina; 1% Ecuador; 7% Minas gerais, Brazil; Yes No data Yes [13] DALY: 2–5 ×106

Taenia solium, cysticercosis

Yes [63–65] Infrequent Only one signi cant report in India. One report in immunosuppressed patient No data

No data

Toxoplasma gondii

Yes [14] Human prevalence in Latin America: Colombia (1.8-2.2%), Brazil (3.0-5.6%), Honduras (15.6-17%), Ecuador (2.6-14.3%), Guatemala (10-17%), Bolivia (22%), Venezuela (4-36.5%). Yes [16–18] Human prevalence: Colombia 47% general population; 60% pregnant women; Perú 58% in pregnant women; Brazil 50% to 76%, Chile 36,9%; Argentina: Human prevalence Ciudad de Buenos Aires, Pregnant women 47.3%. Provincia de Buenos Aires 51.7%, Provincia de Jujuy 39.7%, Provincia de Santa Fe 42.2%, Ciudad de Resistencia 28.5%, Provincia de Chaco 23.8%. Yes [19, 20] Newborn: 0.2% to 2% Immunosuppressed people; main cause of cerebral disease in HIV infected patients Yes [23] Meat (see Table in Ref. 23) Yes [21, 24] One third of human population infected

Yes [22]

Yes [23] Meat (between 20% to 50% of cases)

ANNEX 8 REGIONAL REPORTS

291

292 Global level Main food source and attribution Disease in humans Yes [1–4, 12] DALYs: The most conservative estimate of number of global DALYs lost is 285 407, with no consideration for disease underreporting. Yes [1–3] Yes [1–5, 7, 9] Meat Eating pork and pork products not sanitary inspected and not properly cooked. Disease severity/main population at risk Main food sources and attributions Yes [1–3] Domestic pigs, wild boars, raw horse meat 100% foodborne transmission Disease severity/ main population at risk Yes [4] Description of clinical symptoms and/or signs, epidemiological data and laboratory aspects of human trichinellosis Yes [15] No data No data No data Yes [25, 26] 10% mortality in acute cases; 41 200 new cases per year – rate of 7.7 per 100 000 inhabitants –14 385 cases of congenital Chagas Yes [27, 28] Açai palm juice Guava juice No data Yes [15] For 2010, global population at risk: 5.023 billion. No data No data

Regional level

Species

Disease in humans

Trichinella spiralis

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Trichuris trichiura

Yes [4–11] Argentina, Buenos Aires Province: Total human cases and 65 outbreaks reported from 01/2000 to 09/2004 were analysed. No. of human cases increased from 908 between 1971 and 1981, to 6919 between 1990 and 2002 Chile: Total cases 2012 and previous incidence description Argentina: Serological survey in blood donors prevalence 8.0% No data

Trypanosoma Yes [25] cruzi More than 7 ×106 people infected in the Americas

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05.

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07. 08.

09.

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11.

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15.

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293

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41.

42.

43.

44.

45.

46. 47.

48.

49. 50. 51. 52. 53.

54.

55.

56.

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295

57. 58.

Cacciò, S.M., Thompson, R.C., McLauchlin, J. & Smith, H.V. 2005. Unravelling Cryptosporidium and Giardia epidemiology. Trends in Parasitology, 21(9): 430–437. Kozubsky, L.E. 2008. Zoonosis parasitarias en poblaciones infantiles. pp. 401–407 in Chapter 45, in: Libro Temas de Zoonosis IV. Buenos Aires Asociación Argentina de Zoonosis. See: http:/ /www.veterinariargentina.com/revista/2009/11/zoonosisparasitarias-en-poblaciones-infantiles/ Gonçalves, A.L., Belizário, T.L., Pimentel, J. de B., Penatti, M.P. & Pedroso, R. dos S. 2011. Prevalence of intestinal parasites in preschool children in the region of Uberlândia, State of Minas Gerais, Brazil. Revista Sciedade Brasiliera de Medicina Tropicale, 44(2): 191– 193. Vidal, S., Toloza, L. & Cancino, B. 2010. [Evolution of the prevalence of enteroparasitoses in Talca-Chile] [Article in Spanish]. Revista Chilena de Infectologia, 27(4): 336-340. Miller, S.A., Rosario, C.L., Rojas, E. & Scorza, J.V. 2003. Intestinal parasitic infection and associated symptoms in children attending day care centres in Trujillo, Venezuela. Tropical Medicine and International Health, 8(4): 342–347. Al-Haddad, A.M. & Baswaid, S.H. 2010. Frequency of intestinal parasitic infection among children in Hadhramout governorate (Yemen). Journal of the Egyptian Society of Parasitology, 40(2): 479–488. Mirdha, B.R. & Samantray, J.C. 2002 .Hymenolepis nana: A common cause of paediatric diarrhoea in urban slum dwellers in India. Journal of Tropical Pediatrics, 48(6): 331–334. Al-Megrin, W.A. 2010. Intestinal parasites infection among immunocompromised patients in Riyadh, Saudi Arabia. Pakistan Journal of Biological Sciences, 13(8): 390–394. Gupta, A., Upadhay, B.K., Khaira, A., Bhowmik, D. & Tiwari, S.C. 2009. Chronic diarrhea caused by Hymenolepis nana in a renal transplant recipient. Clinical and Experimental Nephrology, 13(2): 185–186. Kheirandish, F., Tarahi, M., Haghighi, A., Nazemalhosseini-Mojarad, E. & Kheirandish, M. 2011. Prevalence of intestinal parasites in bakery workers in Khorramabad, Lorestan, Iran. Iranian Journal of Parasitology, 6(4): 76–83. Babiker, M.A., Ali, M.S. & Ahmed, E.S. 2009. Frequency of intestinal parasites among food-handlers in Khartoum, Sudan. East Mediterranean Health Journal, 15(5): 1098–1104. Sithithaworn, P., Sukavat, K., Vannachone, B., Sophonphong, K., Ben-Embarek, P., Petney, T. & Andrews, R. 2006. Epidemiology of food-borne trematodes and other parasite infections in a shing community on the Nam Ngum reservoir, Lao PDR. Southeast Asian Journal of Tropical Medicine and Public Health, 37(6): 1083–1090. Gallego, M.L., Gómez Marín, J.E., Torres, E. & Lora, F. 2003. Prevalencia de Entamoeba histolytica en asentamiento temporales post-terremotos en la ciudad de Armenia. Infectio – Revista de la Asociación Colombiana de Infectología, 7(4): 190–194. Guzmán, C.E, López, M.C., Reyes, P., Gómez, J.E., Corredor, A. & Agudelo, C. 2001. Diferenciación de Entamoeba histolytica y Entamoeba dispar en muestras de materia fecal por detección de adhesina de E. histolytica mediante ELlSA. Comunicación breve. Biomedica,; 21(2): 167–171. Pinilla, A.E., López, M.C., Castillo, B., Murcia, M.I., Nicholls, R.S., Duque, S. & Orozco, L.C. 2003. Enfoque clínico y diagnóstico del absceso hepático. [A diagnostic approach to hepatic abscess] [Article in Spanish]. Revista Medica de Chile, 131(12): 1411–1420. Ximénez, C., Morán, P., Rojas, L., Valadez, A. & Gómez, A. 2009. Reassessment of the epidemiology of amebiasis: state of the art. Infection, Genetics and Evolution, 96(6): 1023– 1032. Tengku, S.A. & Norhayati, M. 2011. Public health and clinical importance of amoebiasis in Malaysia: a review. Tropical Biomedicine, 28(2): 194–222. Blessmann, J., Van Linh, P., Nu, P.A., Thi, H.D., Muller-Myhsok, B., Buss, H. & Tannich, E. 2002. Epidemiology of amebiasis in a region of high incidence of amebic liver abscess in central Vietnam. American Journal of Tropical Medicine and Hygiene, 66(5): 578–583.

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62.

63. 64. 65.

66.

67. 68.

69.

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71.

72.

73. 74.

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75.

Ben Ayed, S., Ben, A.R., Mousli, M., Aoun, K., Thellier, M. & Bouratbine, A. 2008. Molecular di erentiation of Entamoeba histolytica and Entamoeba dispar from Tunisian food handlers with amoeba infection initially diagnosed by microscopy. Parasite, 15(1): 65– 68. Esteban, J.G., Aguirre, C., Angles, R., Ash, L.R. & Mas-Coma, S. 1998. Balantidiasis in Aymara children from the northern Bolivian Altiplano. American Journal of Tropical Medicine and Hygiene, 59(6): 922–927. Schuster, F.L. & Ramirez-Avila, L. 2008. Current world status of Balantidium coli. Clinical Microbiology Reviews, 21(4): 626–638. Sharma, S. & Harding, G. 2003. Necrotizing lung infection caused by the protozoan Balantidium coli. Canadian Journal of Infectious Disease, 14: 163–166. Eckert, J., Gemmell, M.A., Meslin, F.-X. & Pawlowski, Z.S. (Editors). 2001. WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. World Health Organization (WHO), Geneva, Switzerland, and World Organisation for Animal Health (OIE), Paris, France. 265 p. Larrieu, E., Belloto, A., Arambulo III, P. & Tamayo, H. 2009. Echinococcosis quística: epidemiología y control en América del Sur. Parasitologia Latinoamericana, 59: 82–89. Guarnera, E.A. 2009. Hidatidosis en Argentina: carga de enfermedad. 1a ed. Organización Panamericana de la Salud - OPS. Buenos Aires, Argentina. 87 p. Available at http:/ / publicaciones.ops.org.ar/publicaciones/otras%20pub/pubhidatidosis.pdf Ministerio De Salud De La Nacion.. 2012. Secretaria De Promoción Y Programas Sanitarios National Report. Boletín Integrado de Vigilancia, 102 - SE 51: 7–13. Irabedra, P. & Roig, C. 2007. Estimación del impacto económico de la equinococosis quistica en el Cono Sur (Argentina, Brasil, Chile y Uruguay). Organizacion de las Naciones Unidas para la Alimentacion y la Agricultura, O cina Regional para America Latina y el Caribe. Documento FAO/RLC Junio 2007. Pavletic, C. 2004. Situacion de la Hidatidosis en Chile. pp. 34–38, in: Informe del Proyecto Subregional Cono Sur de Control y Vigilancia de la Hidatidosis – Argentina, Brasil, Chile y Uruguay. Primera Reunión Constitutiva. Montevideo, Uruguay, 7 al 9 de julio de 2004. OPS Doc. OPS/DPC/VP/PANAFTOSA/URU-QH.01- 04 See: http:/ /www.bvsops.org.uy/pdf/ equinoc.pdf Paz, F.A.Z. 2004. Situação da hidatidose no Rio Grande do Sul, Brasil. pp. 45–50, in: Informe del Proyecto Subregional Cono Sur de Control y Vigilancia de la Hidatidosis – Argentina, Brasil, Chile y Uruguay. Primera Reunión Constitutiva. Montevideo, Uruguay, 7 al 9 de julio de 2004. OPS Doc. OPS/DPC/VP/PANAFTOSA/URU-QH.01- 04 See: http:/ / www.bvsops.org.uy/pdf/equinoc.pdf Mera y Sierra, R., Agramunt, V.H., Cuervo, P. & Mas-Coma, S. 2011. Human fascioliasis in Argentina: retrospective overview, critical analysis and baseline for future research. A review. Parasites & Vectors, 4: Art. no. 104 [Online; DOI: 10.1186/1756-3305-4-104]

76.

77. 78. 79.

80. 81.

82. 83.

84.

85.

86.

TABLE A8.7.2 Data availability for parasite prevalence or concentration in the main food categories for South America Balantidium coli No substantive data. Blastocystis spp. Vegetables Yes [22] Colombia: 44% tomatoes; 37% carrot; 28% cabbage; 25% onion. Other Yes [22] Colombia: 34% of eggs.

Cyclospora cayetanensis Fruits Yes [23–25] Vegetables Yes [23–25]

ANNEX 8 REGIONAL REPORTS

297

Entamoeba histolytica No substantive data. Giardia spp. No substantive data. Hymenolepis nana No substantive data. Toxoplasma gondii [9–21] Beef Colombia: 48% by PCR Colombia: seroprevalence 35% Brazil: 49.4% seropositive (38/77) in cattle in Rio Janeiro; For comparison: 0% by bioassay in USA Colombia: 29–70% by PCR Erechim, Brazil: 17/50 (34%) samples from the diaphragm and 33/50 (66%) samples from the tongue demonstrated a positive PCR reaction. Colombia: seroprevalence 9–15%. Rio Janeiro, Brazil: seroprevalence 7.64% (31/406) in pigs; 11.5% (7/61) in pigs. Londrina, Brazil: bioassay in mice, 13 (8.7%) sausage samples were positive, in one of them T. gondii was isolated and in the other 12 the mice seroconverted) 1% USA; USA 24–92% by bioassay 40% by PCR (Colombia); Seroprevalence 16% (Colombia); 40% seroprevalence in free range chicken in Espirito Santo, Brazil. Deer: 21%-27% by bioassay (USA) Sheep: 4-77% (bioassay, USA); Brasil seroprevalence 1980–2011: 18.6% São Paulo to 61% Minas Gerais

Pork

Poultry Game Other

Trichinella spiralis [1–8] Pork Argentina: in 11.7% of 1128 human cases the suspected food was pork meat and derivatives 1–150 larvae per gram. Argentina: pigs in Buenos Aires Province studied by DAR had 2.07% prevalence, with worm burdens 8.4–105.6 larvae per gram of muscle. ELISA serology prevalence 20–21% Argentina: Muscle larvae of Trichinella from infected animals were identi ed at the species level by PCR in 38 of 56 pork products. Argentina: 300 pigs slaughtered in Rio Negro province 2000–2002 had prevalence (DAR) of 4.8–7.3%. ELISA serology prevalence in 181 animals 19.9%. Argentina: Trichinella spp. from a sylvatic cycle caused human outbreaks due to eating meat from puma, armadillo and wild boar. Chile: human trichinosis from eating roast wild boar (Sus scrofa)

Game

Trypanosoma cruzi Fruits Yes [7, 8] Experimental infection. In outbreak oral transmission by juice fruits considered the most important origin.

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References for Table A8.7. 2 01. Bolpe, J., Ledesma, M., Benitez, M., Cechini, D. & Gonzales Ayala, S. 2005. Human trichinellosis in Argentina. Clinical Microbiology and Infection, 11 (Suppl. 2): 46–47 [Abstract only]. Ribicich, M., Gamble, H.R., Rosa, A., Bolpe, J. & Franco, A. 2005. Trichinellosis in Argentina: an historical review. Veterinary Parasitology, 132(1-2): 137–142. Ribicich, M., Gamble, H.R., Bolpe, J., Scialfa, E., Mundo, S., Pasqualetti, M., Cardillo, N., San Martin, C., Vizio, E., Borrás, P., Fariña, F. & Rosa, A. 2011. Diagnosis of trichinellosis by elisa test with three types of antigens of Trichinella spiralis in pigs raised under di erent conditions of con nement. The Pig Journal, 66: 55–58. Krivokapich, S.J., Molina, V., Bergagna, H.F. & Guarnera, E.A. 2006. Epidemiological survey of Trichinella infection in domestic, synanthropic and sylvatic animals from Argentina. Journal of Helminthology, 80(3): 267–269. García, E., Mora, L., Torres, P., Jercic, M.I. & Mercado, R. 2005. First record of human trichinosis in Chile associated with consumption of wild boar (Sus scrofa). Memorias do Instituto Oswaldo Cruz, 100(1): 17–18. Larrieu, E., Molina, V., Albarracín, S., Mancini, S., Bigatti, R., Ledesma, L., Chiosso, C., Krivokapich, S., Herrero, E. & Guarnera, E. 2004. Porcine and rodent infection with Trichinella, in the Sierra Grande area of Rio Negro province, Argentina. Annals of Tropical Medicine and Parasitology, 98(7): 725–731. Cardoso, A.V., Lescano, S.A., Amato Neto, V., Gakiya, E. & Santos, S.V. 2006. Survival of Trypanosoma cruzi in sugar cane used to prepare juice. Revistra do Instituto de Medicina Tropical de Sao Paulo,; 48: 287–289 Nóbrega, A.A., Garcia, M.H., Tatto, E., Obara, M.T., Costa, E., Sobel, J. & Araujo, W.N. 2009. Oral transmission of Chagas disease by consumption of açaí palm fruit, Brazil. Emerging Infectious Diseases, 15(4): 653–655. Lora, F., Aricada, H., Pérez, J.E., Arias, L.E., Idarraga, S.E., Mier, D. & Gómez Marín, J.E. 2007. Detección de Toxoplasma gondii en carnes de consumo humano por la técnica de reacción en cadena de la polimerasa (PCR) en tres ciudades del eje cafetero. Infectio, 11(3): 117–123. Riddell, P., Daguer, H., Trigueiro, R., da Costa, T., Lustoza, A., Gatti, L. & Reis, M.R. 2004. Soroprevalência de anticorpos anti-Toxoplasma gondii em bovinos e funcionários de matadouros da microrregião de Pato Branco, Paraná, Brasil. Ciência Rural, 34: 1133–1137. Available at: http:/ /www.scielo.br/pdf/cr/v37n1/a50v37n1.pdf Pérez, J.E., Aricapa, H.J., Candelo, S.M., Guevara, L.A., Meza, J.A. & Correa, R.A. 2006. Prevalencia de anticuerpo anti-Toxoplasma gondii en cuatro especies de consumo humano en Caldas - Colombia. Biosalud, 5: 33–42. Luciano, D.M., Menezes, R.C., Ferreira, L.C., Nicolau, J.L., das Neves, L.B., Luciano, R.M., Dahroug, M.A. & Amendoeira, M.R. 2011. Occurrence of anti-Toxoplasma gondii antibodies in cattle and pigs slaughtered, State of Rio de Janeiro. Revista Brasiliera de Parasitologia Vetinaria, 20(4): 351–353. Frazão-Teixeira, E. & de Oliveira, F.C. 2011. Anti-Toxoplasma gondii antibodies in cattle and pigs in a highly endemic area for human toxoplasmosis in Brazil. Journal of Parasitology, 97(1): 44–47. Jones, J.L. & Dubey, J.P. 2012. Foodborne toxoplasmosis. Clinical Infectious Diseases, 55(6): 845–851. Belfort-Neto, R., Nussenblatt, V., Rizzo, L., Muccioli, C., Silveira, C., Nussenblatt, R., Khan, A., Sibley, L.D. & Belfort, R. Jr. 2007. High prevalence of unusual genotypes of Toxoplasma gondii infection in pork meat samples from Erechim, Southern Brazil. Anais da Academia Brasiliera de Ciencas, 79(1): 111–114. Dias, R.A., Navarro, I.T., Ru olo, B.B., Bugni, F.M., Castro, M.V. & Freire, R.L. 2005. Toxoplasma gondii in fresh pork sausage and seroprevalence in butchers from factories in Londrina, Paraná State, Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo, 47(4): 185–189.

02. 03.

04.

05.

06.

07.

08.

09.

10.

11.

12.

13.

14. 15.

16.

ANNEX 8 REGIONAL REPORTS

299

17.

Fialho, C. & Pacheco, F.A. 2003. Detecção de anticorpos para Toxoplasma gondii em soro de suínos criados e abatidos em frigorí cos da região da grande Porto Alegre-RS, Brasil. [Detection of antibodies against Toxoplasma gondii in sera from swine bred and slaughtered in the greater Porto Alegre-RS abbattoirs, Brazil. In Brazilian] Ciencia Rural, 33: 893–897. See: http:/ /www.scielo.br/pdf/cr/v33n5/17136.pdf Dubey, J.P., Gomez-Marin, J.E., Bedoya, A., Lora, F., Vianna, M.C., Hill, D., Kwok, O.C., Shen, S.K., Marcet, P.L. & Lehmann, T. 2005. Genetic and biologic characteristics of Toxoplasma gondii isolates in free-range chickens from Colombia, South America. Veterinary Parasitology, 134(1-2): 67–72. Beltrame, M.A., Pena, H.F., Ton, N.C., Lino, A.J., Gennari, S.M., Dubey, J.P. & Pereira, F.E. 2012. Seroprevalence and isolation of Toxoplasma gondii from free-range chickens from Espírito Santo state, southeastern Brazil. Veterinary Parasitology, 188(3-4): 225–230. Chun-Hsuan Wang, C.-H., Kliebenstein, J., Hallam, A., and 9 others. 2001. Levels of Toxoplasma gondii in swine operations. Iowa State University, USA, Health/Food Safety report. Available at: http:/ /www.ipic.iastate.edu/reports/00swinereports/asl-693.pdf [Accessed 2013-04-09] Andrade, M. 2012. Prevalência da toxoplasmose em ovinos e caracterização molecular de isolados de Toxoplasma gondii (Nicolle & Manceaux, 1909) obtidos de animais de produção no Estado do Rio Grande do Norte. Tese, Departamento de Parasitologia do Instituto de Ciências Biológicas da Universidade Federal de Minas Gerais, Brazil. Available at: http:/ / www.bibliotecadigital.ufmg.br/dspace/bitstream/handle/1843/BUOS-8VVKDT/1_ tese_11_5_12_vers_o_ nal_.pdf?sequence=1 Londoño, A.L., Lora, F., Loaiza, J., Rivera, R. & Gomez, J.E. 2010. Blastocystis sp. en fuentes ambientales y relación con infección sintomática en población infantil, Calarcá, Quindío. Poster presentation KO-25 in: Memorias VII Encuentro Nacional de Investigación en Enfermedades Infecciosas. Asociación Colombiana De Infectología, Revista Infectio, 14(Suppl. 1): 57. Available at: http:/ /www.scielo.org.co/pdf/inf/v14s1/v14s1n3.pdf

18.

19.

20.

21.

22.

TABLE A8.7.3 Data availability for risk management options for each parasite-commodity combination for South America NOTE: The authors were asked to consider all combinations of the particular parasite and the main food categories, namely Beef, Dairy, Pork, Poultry, Game, Seafood, Fruit, Vegetables and Other.

Echinococcus granulosus (See refs 13–14) Beef In endemic areas of Argentina, Chile, Uruguay, Brazil and Peru: Control programmes with systematic de-worming of rural dogs, improvement of family slaughter of sheep and pigs for human consumption, avoiding feeding dogs with raw viscera, and health education of rural inhabitants. In endemic areas of Argentina, Chile, Uruguay, Brazil and Peru: Control programmes with systematic de-worming of rural dogs, improvement of family slaughter of sheep and pigs for human consumption, avoiding feeding dogs with raw viscera, and health education of rural inhabitants. In endemic areas of Argentina, Chile, Uruguay, Brazil and Peru: Control programmes with systematic de-worming of rural dogs, improvement of family slaughter of sheep and pigs for human consumption, avoiding feeding dogs with raw viscera, and health education of rural inhabitants.

Pork

Vegetables

300

MULTICRITERIA BASED RANKING FOR RISK MANAGEMENT OF FOOD BORNE PARASITES

Toxoplasma gondii (See refs 10–12) Beef Pre harvest: remove cat from farm; reduce or prevent oocyst shedding contamination; sterilize feed and bedding; no outdoor access; reduce exposure to oocysts. Toxoplasma-infected rodents: rodent control programme; reduce transmission of Toxoplasma to omnivorous meat animals. Tissue cysts in meat: post-harverst. Irradiation at 0.4–0.7 kGy or high-pressure processing at 300–400 MPa can inactivate T. gondii tissue cysts in meat. However, the e ects of irradiation on colour and of high pressure treatment on colour and texture have limited consumer acceptance. Freezing meat to an internal temperature of -12°C kills T. gondii tissue cysts. Salting, curing, smoking, and the addition of solutions to meat to enhance colour and taste can reduce the viability of T. gondii in meat. However, there is too much variability in these procedures to make a safety recommendation. Pre harvest: remove cat from farm; reduce or prevent oocyst shedding contamination; sterilize feed and bedding; no outdoor access; reduce exposure to oocysts. Toxoplasma-infected rodents: rodent control programme; reduce transmission of Toxoplasma to omnivorous meat animals. Tissue cysts in meat: post-harverst. Irradiation at 0.4–0.7 kGy or high-pressure processing at 300–400 MPa can inactivate T. gondii tissue cysts in meat. However, the e ects of irradiation on colour and of high pressure treatment on colour and texture have limited consumer acceptance. Freezing meat to an internal temperature of -12°C kills T. gondii tissue cysts. Salting, curing, smoking, and the addition of solutions to meat to enhance colour and taste can reduce the viability of T. gondii in meat. However, there is too much variability in these procedures to make a safety recommendation. Pre harvest: remove cat from farm; reduce or prevent oocyst shedding contamination; sterilize feed and bedding; no outdoor access; reduce exposure to oocysts. Toxoplasma-infected rodents: rodent control programme; reduce transmission of Toxoplasma to omnivorous meat animals. Tissue cysts in meat: post-harverst. Irradiation at 0.4–0.7 kGy or high-pressure processing at 300–400 MPa can inactivate T. gondii tissue cysts in meat. However, the e ects of irradiation on colour and of high pressure treatment on colour and texture have limited consumer acceptance. Freezing meat to an internal temperature of -12°C kills T. gondii tissue cysts. Salting, curing, smoking, and the addition of solutions to meat to enhance colour and taste can reduce the viability of T. gondii in meat. However, there is too much variability in these procedures to make a safety recommendation.

Pork

Poultry

ANNEX 8 REGIONAL REPORTS

301

Trichinella spiralis (See refs 1–9) Pork Recommended methods for monitoring Trichinella in domestic and wild animals for human consumption Trichinella control at all levels (farm, slaughterhouse and processed meats) Breeding improvement Recommended methods for monitoring Trichinella in domestic and wild animals for human consumption Trichinella control at all levels (farm, slaughterhouse and processed meats) Breeding improvement

Game

Sources used for Table A8.7.3 01. Gamble, H.R., Bessonov, A.S., Cuperlovic, K., Gajadhar, A.A., van Knapen, F., Noeckler, K., Schenone, H. & Zhu, X. 2000. International Commission on Trichinellosis: recommendations on methods for the control of Trichinella in domestic and wild animals intended for human consumption. Veterinary Parasitology, 93(3–4): 393–408. Gamble, H.R., Pozio, E., Bruschi, F., Nöckler, K., Kapel, C.M. & Gajadhar, A.A. 2004. International Commission on Trichinellosis: recommendations on the use of serological tests for the detection of Trichinella infection in animals and man. Parasite, 11(1): 3–13. Ribicich, M., Gamble, H.R., Bolpe, J., Sommerfelt, I., Cardillo, N., Scialfa, E., Gimenez, R., Pasqualetti, M., Pascual, G., Franco, A. & Rosa, A. 2009. Evaluation of the risk of transmission of Trichinella in pork production systems in Argentina. Veterinary Parasitology, 159(3-4): 350–353. Ribicich, M., Miguez, M., Franco,A., Basso, N., Gamble, R.H., Santillan, S., Molina,V. & Guanera, E. 2000. Evaluation of ELISA test for the diagnosis of porcine trichinellosis. The Pig Journal, 46: 24–34. OIE (World Organisation for Animal Health). 2012. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Chapter 2.1.6. Trichinellosis. [Version adopted by the World Assembly of Delegates of the OIE in May 2012]. 9 p. See: http:/ /www.oie.int/ leadmin/Home/eng/ Health_standards/tahm/2.01.16_TRICHINELLOSIS.pdf Guarnera, E.A., Molina, V.E. & Krivokapich, S.J. 2007. Vigilancia epidemiológica in vivo de la trichinellosis porcina en cerdos expuestos naturalmente a la enfermedad. pp. 112–116, in: Seminario nal del proyecto TCP 3003 – Mejoramiento del Control de la Trichinellosis. 5 de octubre de 2006, Instituto de Patobiología, INTA Castelar, Argentina. FAO, Rome, Italy. Murrell, K.D. 2007. Trichinellosis. The Global Situation and Prospects for Complete Control. pp. 110–111, in: Seminario nal del proyecto TCP 3003– Mejoramiento del Control de la Trichinellosis. 5 de octubre de 2006, Instituto de Patobiología, INTA Castelar, Argentina. FAO. Rome, Italy. van Knapen, F. 2000. Control of trichinellosis by inspection and farm management practices. Veterinary Parasitology, 93(3-4): 385–392. Nöckler, K., Pozio, E., Voigt, W.P. & Heidrich, J. 2000. Detection of Trichinella infection in food animals. Veterinary Parasitology, 93(3-4): 335–350. Kijlstra, A. & Jongert, E. 2009. Toxoplasma-safe meat: close to reality? Trends in Parasitology, 25(1): 18–22. Kijlstra, A. & Jongert, E. 2008. Control of the risk of human toxoplasmosis transmitted by meat. International Journal for Parasitology, 38(12): 1359–1370 Jones, J.L. & Dubey, J.P. 2012. Foodborne toxoplasmosis. Clinical Infectious Diseases, 55(6): 845–851. Eckert, J., Gemmell, M.A., Meslin, F.-X. & Pawlowski, Z.S. (Editors). 2001. WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. World Health Organization (WHO), Geneva, Switzerland, and World Organisation for Animal Health (OIE), Paris, France. 265 p. Ministerio de Salud de la Nacion. 2009. Norma técnica y manual de procedimientos para el control de la hidatidosis en la República Argentina.

02.

03.

04.

05.

06.

07.

08. 09. 10. 11. 12. 13.

14.

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I nfectious diseases caused by food-borne parasites h ave not receive d th e same leve l of attention as oth er food-borne biological and ch emical h aza rds. N eve rth eless, th ey cause a h igh burden of disease in h umans, may h ave prolonged, seve re, and sometimes fatal outcomes, and result in considerable h ardsh ip in terms of food safety , security , q uality of life, and negative impacts on live lih oods. T h e transmission routes for food-borne parasites are dive rse. T h ey can be transmitted by ingesting fresh or processed foods th at h ave been contaminated via the environment, by animals or people. Additionally, notification to public h ealth auth orities is not compulsory for most parasitic diseases, so official reports do not capture the true prevalence or incidence of th e diseases, as much underreporting occurs. T h is report presents th e results of a global ranking of food-borne parasites from a food safety perspective . I t also provi des an ove rvi ew of th e current status of know ledge of th e ranked parasites in food and th eir public h ealth and trade impact, and provi des advi ce and guidance on th e parasite-commodity combinations of particular concern, th e issues th at need to be addressed by risk managers, and th e risk management options ava ilable to th em. I t documents th e ranking process used to facilitate its adoption at regional, national, or local leve ls. T h is vo lume and oth ers in th is Microbiological Risk Assessment Series contain information th at is useful to both risk assessors and risk managers, th e C odex A limentarius C ommission, gove rnments and regulatory agencies, food producers and processers and oth er institutions or indivi duals w ith an interest in foodborne parasites and th eir impact on food safety , public h ealth and live lih oods.

Основные сведения

Организация Всемирная организация здравоохранения (ВОЗ / WHO)

Тип документа Publications

Дата принятия 30 апреля 2014 г.

Источник Всемирная организация здравоохранения