Epidemiology of foodborne diseases : a worldwide review / Ewen C. D Todd

Epidemiology of foodborne diseases: a worldwide review Ewen C. D. Todda

Introduction Every society has some interest in food safety and disease control. Mter the Second World War, governments had shifted away from addressing public health problems with communicable diseases to long-term effects of chemicals in the food supply, because it was thought that infectious diseases were under control. In the last decade, however, there has been a change in food safety priorities from chemical issues back to microbial hazards, at least in North America. This is due to the recognition of new life-threatening agents, the occurrence of continuing well-publicized outbreaks transmitted through food and water, and the apparent inability of public health authorities to prevent them. The current concerns are raw foods of animal origin and fresh produce contaminated by Escherichia coli 0157:H7, Listeria monocytogenes and Salmonella, along with enteric viruses in shellfish and parasites such as Toxoplasma, Cryptosporidium and Cyclospora in meat and fruit. Also, traditional pathogens have been recognized as causing illnesses from new foods, such as Salmonella in melons and Clostridium botulinum in garlic bottled in oil. However, although reporting is improving, it is still very limited. The number of cases of enteric illnesses based on laboratory isolations of pathogens from stool specimens has been underestimated by a factor of 20 to 100 (1). In addition, for most of these no source of infection is identified. Despite these limitations, some countries have been collecting and reporting data for years and increasing numbers of others are starting the process. However, foodborne disease cases are significantly underestimated, and relatively few well-investigated outbreaks are described although these usually give information on the etiological agent and the reason for the contamination. Therefore, no national system has yet determined accurately the extent of foodborne diseases, and data from different countries may show distinct differences which may reflect as much the way that these are collected and interpreted as the geographic location and food habits of the people. Thus, caution must be advised in making too critical a comparison of food borne disease statistics from nation to nation. This in-

creasing commitment to the documentation and control of foodborne disease indicates an awakening awareness to its significance in terms of morbidity, mortality, economic loss, and effects on trade between countries and common markets. The following discussion on worldwide surveillance of foodborne disease updates previous reviews (2, 3).

Objectives of a toodborne disease surveillance system A well-constructed food safety programme for the protection of the population comprises investigation of foodborne disease incidents, laboratory analysis of foods and clinical specimens for pathogens and contaminants, regular inspection of foods and their production chain, appropriate legislation for the prevention of foodborne disease, and education of those working at the different sectors of the food industry and the consumer. Surveillance is necessary to identify foodborne diseases, their causes, and their socioeconomic impact, in order to help determine the best short- and long-term control measures. It should include the systematic collection of relevant incident data, its evaluation for completeness and accuracy, compilation into standard formats, and interpretation of trends with examples from specific outbreaks. There are at least 4 components to a well-designed surveillance system: (i) early alert of disease; (ii) laboratory isolation data; (iii) reports of foodborne illness incidents; and (iv) use of special epidemiological studies and surveys, including sentinel site studies, to determine a more realistic level of morbidity. Surveillance principles are covered more fully by Borgdorff and Motaijemi (4 ). Foodborne disease surveillance is carried out at the local level and reports are actively or passively transferred to a national centre, or at least to a central coordinating body, for standardizing the material and preparing annual or other types of reports. Reports include laboratory isolation data and foodborne disease outbreaks. Specific epidemiological studies may not be coordinated at the national level, but appear in the scientific literature for review. Some countries have a federated system of states, provinces or cantons that take different responsibilities for health care and surveillance. These can enhance a national system but another layer of bureaucracy tends to slow down the reporting. A full discussion on foodborne disRapp. trimest. statist. sanff. mond., 50 (1997)

a

Bureau of Microbial Hazards, Health Protection Branch, Health Canada, Sir Banting Research Centre, Ottawa, Ontario, Canada.

30

ease smveillance is given in Bryan et al. (5, 6), Guzewich et al. (7) and Todd et al. (8). Selected regions of the world are reviewed for their contribution to our knowledge of food borne disease.

Europe Summary of foodborne disease surveillance programme in Europe Since 1980, many European and a few other countries have participated in an early warning and routine reporting system, coordinated through the FAO/WHO Collaborating Centre for Research and Training in Food Hygiene in Berlin (9); by 1996, 46 countries in the WHO European Region had participated in this programme with varying degrees of commitment (10). These reports standardized as much as possible so that data can be compared, but because of the different degrees of commitment to reporting in these countries, direct comparisons of data between countries are questionable. However, some general statements can be made. Where foodborne diseases are notifiable, the incidence rates are increasing for Austria and England/Wales, relatively stable for Spain and Scotland and decreasing for Poland. For salmonellosis, generally rates grew until1992 and decreased slighly in 1993, perhaps indicating the start of more effective control measures against S. enteritidis. In contrast, campylobacteriosis cases appear to be continuing to rise well beyond rates for salmonellosis. Travel abroad to resorts on the Mediterranean Sea and to Asian and Mrican countries was cited as a source for some of these infections. Twenty-one countries specifically reported foodborne outbreaks ranging from 5 (Albania) to 2 818 (Spain) from 1990 to 1991/92. In 19.5% of these outbreaks the agent was unknown or unspecified. Where the agents were identified, Salmonella spp. caused 84.5% of all outbreaks (S. enteritidis 50.9%), Staphylococcus aureus 3.5%, C. peifringens 3.0%, C. botulinum 1.1% and Bacillus cereus 1.0%. All other causative agents were <1% except for Trichinella, (1.5%) and mushrooms (1.3%). The etiology of the outbreaks in 16 of these countries is shown on Table 1. Most campylobacteriosis illnesses are sporadic cases of unknown origin, and relatively few outbreaks were documented (mostly from the United Kingdom). Only 12 E. coli 0157:H7 outbreaks were reported and these were all from England and Wales, although cases and outbreaks are known to have occurred in other countries (11). However, unspecified E. coli outbreaks were recorded in Germany, the Netherlands, Romania, Spain and Scotland, and some of these were probably Verotoxin-producing strains (VTEC) in origin. Trichinosis outbreaks were documented in Lithuania (146), Bulgaria (18), Spain (16) and Wld hlth statist.

France ( 1), and many cases in Romania ( 4 705) and Poland (738). Outbreaks of mushroom poisonings were reported in Hungary ( 158) and Israel ( 1). The most frequent foods associated with outbreaks, where these were identified, were eggs and egg products (25.4%), meat and meat products (23.4%), confectionery, sweets, cakes, pastry, puddings, desserts and ice cream (17.0%). Fish and shellfish, milk and dairy products, and poultry and poultry products were each implicated in less than 5% of outbreaks. There have been limited attempts by countries in this report to associate agents with foods, but there is evidence that Salmonella enteritidis infections have arisen from the consumption of raw or undercooked eggs in a variety of products, and poultry. E. coli 0157 infections have been linked to beef, milk and yoghurt. A few Campylobacter outbreaks were associated with undercooked chicken and meat, unpasteurized milk, and bottled milk pecked by birds. Where the place of contamination or mishandling was clearly identifiable, the farm was where the pathogens were most frequently identified as entering the food chain (50%), with subsequent mishandling mainly at restaurants (22%), homes (13%) and catering establishments (7%). Outbreaks occurred from people eating in homes (46%), restaurants/hotels ( 15%), catered events (8%), medical care facilities and canteens (6% each), and schools (5%). Factors contributing to outbreaks were identified in 7 countries in 55% of outbreaks. Temperature abuse, particularly inadequate cooling and improper cooking, was responsible in 44% of these, contaminated or toxic raw products in 16%, contamination by personnel or equipment in 15%, lack of hygiene in processing, preparing and handling in 10%, and cross-contamination in 4%. The above data are more detailed than in previous reports and are indicative of an increasing commitment to the documentation of foodborne disease in the contributing countries which may eventually lead to control. A few examples at the national level will be given for annual numbers oflaboratory-confirmed and notifiable cases, outbreaks of foodborne disease, and data on specific outbreaks.

Specific epidemiological studies In Denmark, there was a very gradual decrease in cases of campylobacteriosis and yersiniosis, but for salmonellosis there were two distinct peaks in 1989 and 1992 (Table 2). The increase in 1992 was mainly due to S. enteritidis and S. typhimurium (a phage type found in pigs). The notifiable foodborne and waterborne disease cases increased steadily between 1984 (192) and 1992 (1 189) with a slight peak in 1988 and a profile similar to that for salmonellosis, indicating that many of the foodborne diseases may have been caused by Salmonella. 31

quart., 50 (1997)

Table 1 Foodborne disease in 16 countries by percentage of outbreaks of known etiology, WHO Region for Europe Tableau 1 Maladies d'origine alimentaire dans 16 pays, en pourcentage des flambees d'etiologie connue, Region europeenne de I'OMS Etiology- Etiologie AlbaniaAlbanie 1990-91 Bulgaria- DenmarkBulgane Danemark 1990-92 1990-92 Finland Fmlande 1990-92 France1990-92 Germany- HungaryAllemagne Hongne 1990-92 1990-92 Icelandlslande 1985-93 IsraelIsrael 1990-92

MaltaMalte 1990-93

Bacillus cereus Campylobacter Clostridium botulinum Clostridium perfringens Salmonella 100 Shigella Staphylococcus aureus Other bacterial b- Autres bacteries b Total bacterial (%) - Total des etiologies bacteriennes (%) 1DD Viral- Virus Seafood toxins- Toxines de poissons et fruits de mer Plant - Vegetaux Chemical - Produits chimiques Parasitic - Parasites Other - Divers Total number of outbreaks Nombre total de llambees Et1ology - Etlologie

6

13

3 3

6 12 66

2

26 4 19 33 19

4 18

7 3

33

5 85

38 14

29 16

2 88

73 <1

1

<1 2

6

7

9 2

21 7 18 16

81

11

73

76 1

93

98 <1 2

97 3

76

1DD

8D

96

4 4

7

24 <1 <1 <1

7

27 6

5 2 12 2

4

3

67

69

55 Portugal1990-91

1 666 RomaniaRoumanie 1990-92

319 SpalnEspagne 1990-92

648 SwedenSuede 1990-92

27

56 England and WalesAng leterre et Pays de Galles 1992-93

27 ScotlandEcosse 1990-92

NetherlandsPays-Bas 1990-91

Bacillus cereus Campylobacter Clostridium botulinum Clostridium perfringens Salmonella Shigella Staphylococcus aureus Other bacterialb- Autres bacteriesb Total bacterial (%) - Total des etiologies bacteriennes (%) Viral -Virus Seafood toxins- Toxines de poissons et fruits de mer Plant - Vegetaux Chemical - Produits chimiques Parasitic - Parasites Other - Divers Total number of outbreaks Nombre total de flambees

25

2

<1 7 17 17 3 1

3 3 17

2 17

<1 11

2

34 59

57 2

84 <1 6 2

10

24 13

27 96 1DD

51 5 12 7

68 <1 2

85

2

1DD

96

98 2

93 6

99

4 2

59

29

125

1723

6D

4D3

486

• Source: 6th Report of the WHO Surveillance Programme (Ref. 10).-6' Rapport du Programme OMS de Surveillance {Ref. 10). b "Other bactenal" refers to E. col;, 1n the case of England & Wales and Scotland 1t is specified whether VTEC or 0157:H7.- «Autres bactenes• designe E. coli; pour I'Angleterre et le pays de Galles et pour I'Ecosse, il est precise qu'il s'ag1t de VTEC ou de 0157:MH7.

32

Rapp. trimest. statist. sanit. mond., 50 (1997)

Table 2 Cases of enteric disease in Denmark, 1988-1992a Tableau 2 Cas de maladies intestinales au Danemark, 1988-1992a Disease- Maladie Campylobacteriosisb - Campylobacterioseb Salmonellosisb - Salmonelloseb Yersiniosisb - Yersinioseb Foodborne and waterborne diseasescMaladies d'origine alimentaire et hydriquec • Source: 6th b

1988 1 276 3 200 865 1 123

1989 1 432 3 500 879 926

1990 1 367 2 081 817 898

1991 1 261 2 203 929 954

1992 1 129 3 373 909 1 189

Mean no./1 00 000 in 1992 N moyen/1 00 000 en 1992 22 65 18 23

c

Report of the WHO Surveillance Programme (Ref. 10). -6• Rapport du Programme OMS de Surveillance (Ref. 10). Laboratory-confirmed cases.- Cas confirmes au laboratoire. Notifiable cases.- Cas adeclaration obligatoire.

In Germany, there are fewer Campylobacterjejuni cases reported than for Salmonella, unlike other European countries, but campylobacteriosis is considered an important disease (10, 12). A survey showed that 10.9% of 485 retail food samples surveyed contained the organism- turkey liver 66%; poultry 50%; milk/milk products 2.9%; fish 2.3%; meat products 0.8%; shellfish and sausage 0% (12). Deep frozen, raw products were more frequently contaminated than fresh, raw products (23.8% vs. 12.4%). In Switzerland, a case-control study showed that most infections were caused by Salmonella enteritidis PT 4 (13), and associated with the consumption of raw or undercooked eggs, especially in desserts made with raw eggs. Infections from other serovars were more likely to be contracted in other countries and were not associated with eggs. VTEC seem to be a major cause of haemolytic uraemic syndrome (HUS). Children with this disease in the Czech Republic had evidence ofVIEC infection (verotoxin in stools, antibodies to E. coli LPS in sera, or isolation of VTEC strains) (14). Serotypes 026:Hll and 0157 were the most frequently isolated. However, no source of the infections was identified. In the Netherlands, Belgium and Germany, 78% of HUS patients had evidence ofVIEC infections (15). E. coli 0157 was the most frequent causative agent and VI-2 the most frequent toxin produced. Where E. coli 0157 was isolated in family members, the strains were identical by subtyping analysis. In Scotland after 13 years of experience with 0157 infections, the epidemiology is becoming better understood ( 16). The outbreaks have been associated with ground meat, unpasteurized milk, unpasteurized milk farm cheese, contaminated pasteurized milk, vegetables fertilized with cow manure, drinking and recreational water supplies, and person-to-person spread. Livestock, particularly cattle, are considered to be major reservoirs of this group of organisms. Wld hlth statist. quart., 50 (1997)

One of the reasons for the establishment of the international Salm-Net programme was to identify trends in salmonellosis in Western Europe. Between 1993 and 1995 there was a fall of 6.8% in all isolates in 7 contributing countries, with S. enteritidis and S. typhimurium representing about 75% of these. However, the trend for these two serovars was different; S. enteritidis decreased each quarter by a total of 16.4%, and S. typhimurium rose each quarter during the same 3years by 15.2% (17). The decrease in S. enteritidis may represent efforts to limit infection in flocks and use unheated eggs less frequently in food items. It is also noted that many of the S. typhimuriumstrains are multidrug resistant and this leads to an emerging problem in enteric infections. Salm-Net also aims to type strains beyond their serological designation, and is requesting phage typing for the most common serotypes.

Foodborne disease annual reports In France, the number of outbreaks rose from 594 in 1990 to 732 in 1992. Where the agent was identified, Salmonella was responsible for 83-87% of outbreaks. Eggs and egg products were associated with many outbreaks, particularly after they were contaminated with S. enteritidis (Table 3). Meat and meat products, and also mixed foods, were the important vehicles for causing Salmonella, C. perfringens and S. aureus outbreaks. Most fish- and shellfish-borne outbreaks were caused by histamine and diarrhoeic shellfish poison, respectively. Outbreaks involving dairy products, such as cheese and ice cream, and frequently-handled prepared foods most likely arose from S. aureus intoxication. Outbreaks typically occurred after people had eaten at homes, schools, restaurants, canteens, hospitals and homes for the aged, holiday resorts, prisons and religious gatherings. The contributing factors most commonly documented were contaminated equipment, faults in processing, inadequate cooling, contaminated raw ingredients, preparation 33

Table 3 Food borne disease outbreaks by known etiology and associated foods, France, 1990 -1992a Tableau 3 Flambees de maladies d'origine alimentaire selon l'etiologie et !'aliment associe, France, 1990-1992a YearAnmle 1990 Et1ology EtiologieMeaVpoultryViande/volaille 19(15%) 16 (67%) 4 (16%) 2 (9%) 22 (12%) 15 (68%) 6 (16%) 1 (4%) 13 (7%) 6 (30%) 5 (14%) 1 (8%) Surveillance Programme (Ref. Egg/egg productsCEufs/produils abase d'reufs 91 (71%) 3 (12%) 113 (60%) 2 (5%) 1 (4%) 118 (65%) 5 (14%) 1 (8%) 10).-6• Rapport du

Fish/shellfish- M1lk/da1ry productsPoissons/ LaiVproduits laitiers fruits de mer 6 (5%) 1 (4%) 19 (86%) 5 (2%) 1 (3%) 8 (35%) 10 (6%) 2 (6%) 8 (61%) 11 (32%) 10).

OtherDivers 9 (7%) 8 (33%) 8 (32%) 1 (5%) 41 (22%) 7 (32%) 16 (43%) 13 (57%) 39 (22%) 14 (70%) 12 (34%) 3 (23%)

Total

1991

1992

Salmonella C. perfringens S. aureus Other- Divers Salmonella C. perfringens S. aureus Other- Divers Salmonella C. perfringens S. aureus Other- Divers

3 (2%) 9 (36%) 7 (4%) 12 (32%)

128 (100%) 24 (100%) 25 (100%) 22 (100%) 188 22 37 23 (100%) (100%) (100%) (100%)

180 (100%) 20 (100%) 35 (100%) 13 (100%)

• Source: 6th Report of the WHO

Programme OMS de Surveillance (Ref.

too far in advance of eating and contamination through personnel.

Foodborne disease outbreaks Powdered infant formula was responsible for 48 known cases of salmonellosis in infants under 7 months old from 14 regions in Spain fromJanuary to June, 1994 (18). The implicated strain was a lactose-fermenting S. virchow. It took some time for the illnesses to be linked with the Salmonella in the milk powder and recalls to be made. Interestingly, in 1993 a lactose-fermenting S. tennessee in powdered milk products caused infant illnesses in the United States and Canada. Five persons who were suffering from S. enteritidis PT 4 infection in England had attended the same gym and had consumed a protein-based beverage composed of milk powder and a raw egg as a body-building drink ( 19). This is an example of "voluntary" salmonellosis when lifestyle appears to outweigh risks of enteric illness. In Germany, about 1 000 cases of salmonellosis were associated with consumption of paprika and paprika-powdered potato chips (20). The infective dose was 4-45 organisms with an attack rate of 1 in 10 000 exposed persons; several serovars were implicated. This is the largest documented outbreak from contaminated spices. A scombroid outbreak with 15 cases also occurred in Spain from a fresh tuna sold at a supermarket in June 1994 (21). Typical symptoms of facial flushing, headache, diarrhoea, nausea and abdominal pain followed about 45 minutes after a peppery taste was noticed in the tuna. Histamine up to 580 ppm was found in leftover tuna samples, and >35 J.Lg/L in 4 urine specimens from the cases. 34

Although botulism from dairy products is considered rare, some recent outbreaks show that this does occur. In June 1989, the largest outbreak in the United Kingdom took place when commercially prepared hazelnut yogurt was consumed after contamination of the nut paste. In Italy, in August and September, 1996, at least 8 persons and one death resulted after tiramisu made with mascarpone cheese was eaten (22). Most of those ill were children. The cheese contained spores of C. botulinum but it is uncertain how the contamination took place. The widely exported product was recalled on a massive scale. In Scotland, there was a large meatborne E. coli 0157 outbreak with 396 cases and 11 deaths between November 22 and December 11, 1996. Cases had eaten cold cooked meats or meat sandwiches from a butcher or had eaten cooked steak in gravy at a church lunch supplied by the same butcher. This is the second largest foodborne outbreak in Scotland (23), and the latest in a series of outbreaks; it prompted an enquiry into the reason for the dramatic in-crease in food borne disease cases in that country (24). In 1970 there were 858 cases. By 1980 this figure was 2 689; in 1990 and 1995 the numbers were 6 510 and 9 297, respectively, and for 1996, a predicted number of 10 000. The Pennington Report recommended research into prevalence in livestock of E. coli 0157 and more sensitive typing procedures for isolates (24). There should be a more systematic approach to surveillance including electronic reporting and analysis of data. Also, there should be uniform standards of hygiene throughout the food industry. When outbreaks occur a team empowered to take action should quickly be set up. Rapp. trimest. statist. sanit. mond., 50 (1997)

Africa Epidemiological studies and foodborne disease data Little in the way of regular foodborne disease surveillance is done in Mrica, although there is an awareness of the importance of diarrhoea! diseases, and some studies have been carried out. Because food and water are thought to be the main means of transmitting these types of diseases, a survey of hygiene in houses where diarrhoea had occurred was carried out in Liberia (25). Between 40 and 88% of stored water samples contained >103 enterobacteria cfu/100 ml, and 19-32% of adult food samples had >105 enterobacteria cfu/ 100 g. Infant food such as formula, baby cereal and traditional "rice water" were even more contaminated (56% with >105 CFU/100 g) because they had been stored at room temperature for up to 8 hours. In an urban slum community it was a common practice to prepare food in advance of a meal and store it at ambient temperatures for up to 24 hours. It was only occasionally reheated, partly because of lack of fuel. Also, women had only time to make food once per day because they worked far from their homes. Unfortunately, no foods were examined for pathogens. These observations indicate that foodborne and waterborne diseases can be easily spread in such communities and cause a high morbidity. However, a case-control study in Liberia showed that diarrhoea in households was less related to poor food hygiene practices and more to improper disposal of faeces (26). Fortunately, fermented foods, such as those traditionally made in Zimbabwe, are not good vehicles for transmitting pathogens since most pathogens died within a few hours in sour porridge and mahewu because the pH was <3 (27); unfermented porridge (pH 6) allowed the growth of Salmonella, Shigella, enterotoxigenic E. coli (ETEC), and enteropathogenic E. coli (EPEC). Ogi, a fermented maize porridge used for weaning infants in Nigeria, also has a low enough pH to prevent growth of Salmonella and EPEC (28). Another problem with cereal products is contamination by mycotoxins. Moldy grain, which contains aflatoxins, is often consumed under drought conditions. In Kenya and the Sudan, aflatoxins were present in the sera of children suffering from kwashiorkor, but were metabolized in a different way than in children with other forms of malnutrition or normally nourished children (29). The aflatoxins, therefore, may be a contributory factor to kwashiorkor. Another consequence of mouldy food is hepatocellular carcinoma (HCC); levels of aflatoxin B1 have been found as high as 1.5 mg/kg food. There was a strong association with mutations of the p53 gene in HCC and dietary aflatoxin intake in an international study of patients in 14 countries (30). The incidence ofHCC is higher in Mozambique than any other country. Exposure to Toxoplasma gondii is relatively common Wld hlth statist. quart., 50 (1997)

in Mrica with a 18.2-61% prevalence of antibodies in the population of8 countries (31). In the Sudan, both Toxoplasma and Brucella infections are probably associated with consumption of raw liver and intestines (32). In Egypt, the foods at highest risk in 1985 and 1986 were white cheese, fermented cream, meat/ chicken, flour/butter oil, cabbage/rice and potatoes, and many illnesses occurred in homes (33). These food vehicles seemed to be similar to those associated with foodborne disease in Iraq. Between 1983 and 1985 in Egypt, 3 outbreaks from white cheese and 2 from cream/fermented cream were caused by EPEC. Shigella, B. cereus, C. perfringens or C. botulinum, however, were not confirmed as foodborne agents. However, in this country where cereal products are widely eaten, it is probable that at least some mild illnesses arise from consumption of food containing B. cereus enterotoxin, but are not reported. In addition, street-vended food in Egypt has been shown to contain pathogens and many foods awaiting sale were at temperatures favourable for their growth (15-44 °C) (34).

Foodborne disease outbreaks Occasionally, acute illnesses directly associated with a food are documented, such as the following 3 examples. Because of the need to conserve as much meat as possible for human consumption, animals that die unexpectedly may be butchered and eaten. An example of this occurred in 1976 when 155 villagers in Uganda feasted on a zebu cow which was later found to have died from anthrax septicaemia (35). Within 15-72 hours 143 of these villagers developed acute gastroenteritis and 9 children died. Four to five cattle died from anthrax in 1974 and 1975 in the same county where the outbreak occurred. Wild animals such as hippopotamuses and elephants also succumb to the disease, and carcasses may be utilized as human food. Therefore, the potential for more human anthrax poisonings exists. Jimson weed (Datura stramonium) seeds can contaminate grain during harvesting and cause hallucinations from atropine poisoning when ingested. Twenty-two such episodes occurred in the United Republic of Tanzania between 1974 and 1981 involving wheat and millet products (36). In 1991, the first major botulism outbreak with at least 18 deaths arose from ingestion oflocally-made faseikh (uneviscerated fish) (37). In 1994, 3 children died and 6 others suffered from severe diarrhoea caused by E. coli 0157:H7 after eating hamburgers, koshari and dairy products in Egypt. As a follow-up to this, a survey of 175 foods obtained from slaughterhouses, supermarkets and farmers' homes was conducted for E. coli 0157. This pathogen was detected in 6% of unpasteurized milk, 6% of fresh retail beef, 4% ofboneless chicken, and 4% of lamb meat samples (38). 35

Cholera outbreaks have continued to occur in Africa since the seventh pandemic began in 1970. These have caused severe morbidity and mortality in refugee camps in Malawi, Somalia, Ethiopia and the Sudan (39). A study of one outbreak in Malawi in 1988 indicated that there was a common source, which could have been food or water, but no environmental Vibrio isolates were found. Heavy rains destroyed some latrines 15 days before the outbreak, probably contaminating the local water table (39). During 1992, in the Lisungwi refugee camp holding 60 000 Mozambicans, 772 cases of abdominal cramps and bloody diarrhoea were documented (40). The major factor contributing to illness was consumption of cooked food from the market. Based on analysis of stool cultures and the presence of the VT1 gene in some of these, the authors concluded that most of the cases were caused by E. coli 0157:H7 and some by Shigella dysenteriae type 1. The case fatality rate was 4.7%. Refugees are an increasing concern because of civil wars and national conflicts. For instance, 500 000 refugees returned from East Zaire to Rwanda between November 15 and 21, 1996. The epidemiological sentinel stations registered about 14 000 consultations and 4 7 deaths. Diarrhoea! disease accounted for two-thirds of all consultations. The crude mortality rate was estimated at 0.1/10 000/ day (based on the 500 000 denominator). The mortality rate in the Mugunga Camp where the refugee population had stayed earlier was estimated at 0.3/10 000/day (source: WHO data). How much of this diarrhoea! disease is due to food and water is not known, but they are suspected to be major vehicles of enteric pathogens in such situations.

Asia Epidemiological studies and foodborne disease statistics Except for a few countries such as Japan, for instance, relatively little in the way of surveillance of foodborne disease is carried out in Asia, and most information is gleaned from specific but limited investigations and studies. From the number of enteric pathogens isolated from stools of patients in a major hospital in Hong Kong (41), it would seem that the distribution of these pathogens in the population is similar to that in Japan, except that the proportion caused by Shigella is higher and that of Vibrio is lower (Salmonella 52.5%, Campylobacter 16.6%, Shigella 11.3%, Vibrio 5.3% and EPEC 4.4%). Although a link has been made between Campylobacter and Guillain-Barre syndrome (GBS) in the western world (42, 44), this has now also been shown in Kerala State, India (45). From serum samples taken from patients, 26% showed high antibody titres to Campylobacterjejuni and 38% 36

of stool specimens of new GBS cases were positive for C. jejuni/coli. Foodborne campylobacteriosis, therefore, may be very significant from a social and economic point of view globally. Mycotoxins have been responsible for illnesses in 1974 from aflatoxin in maize (15.6 ppm) and in I987 from deoxynivalenol and other trichothecenes in wheat (46, 48). In India and many other Asian countries, cysticerosis from Taenia solium is a major public health problem because the widespread consumption of insufficiently cooked pork (49). A comparative study of food borne outbreaks in the Republic of Korea and Japan between I971 and 1990, conducted by Lee et al. (50), (Tables 4a, 4b, 4c) showed that there were considerable differences in the morbidity and mortality (higher for Japan) and agents involved (Vibrio spp. important in both countries, but more Salmonella than S. aureus associated outbreaks in the Republic of Korea and the converse for Japan). Most incidents occurred in the workplace and the home in the Republic of Korea, whereas it was more in restaurants and hotels in Japan. Seafood was often implicated in both countries, but food of animal origin was much more frequently associated with outbreaks in the Republic of Korea. The authors did not know how much of these differences were due to reporting mechanisms and how much to culture. Pan et al. (51) examined foodborne disease in China (province of Taiwan). From 1987 to 1993 the number of outbreaks reported ranged from 57 to 93. In 1994 there were 102 outbreaks and 4 276 cases. Where the etiology was known, the outbreaks totaled 42 V parahaemolyticus, 15 S. aureus, 11 B. cereus, 6 Salmonella, 1 chemical, and 1 seafood toxin. In particular, the Vibrio outbreaks occurred in the warmer months (April to October). It would appear from this study and that of Lee et al. (50) that the characteristics of outbreaks in China (province of Taiwan) are more similar to those in Japan than in the Republic of Korea. In Vietnam, it was estimated that 30-57% of students in university hostels between 1984 and 1988 suffered from diarrhoea, mainly because food was poorly prepared and stored (52). Street-vended meals in Hanoi in a 1990/91 survey often contained E. coli and C. peifringens. Most of the 5 714 documented illnesses between 1983 and 1988 were caused by Salmonella, E. coli and S. aureus, and 156 of these cases died (fatality rate of 2. 7%). Because anthrax-infected cattle are used for meat, hundreds of persons develop bactaeremia and 3 to 7 die each year (52). Chemical residues in foods are not adequately controlled and many cases are thought to be due to chemical poisonings. Illegal additives deliberately introduced in alcohol, candies, and sweet products have caused intoxications; one such adulterated liquor caused 14 deaths. Foodborne disease was considered to be the most widespread public health problem in Vietnam and Rapp. trimest. statist. sanit. mond., 50 (1997)

Table 4a Food borne disease outbreaks by etiology in the Republic of Korea and Japana Tableau 4a Flambees de maladies d'origine alimentaire, par etiologie, en Republique de Coree et au Japona Country -Pays MorbidityMorb1d1tl!l 100 000

Deaths/cases - Salmonella Deces/cas

S. aureus

Clostridium spp

Vibriospp

E. coli

OtherDivers

Rep. of Korea- Rep.de Coree Japan - Japan

3.0 29.2

2.48% 0.07%

23.1% 14.8%

14.9% 24.8%

0.5% 0.2%

37.6% 47.3%

6.8% 3.5%

17.1% 9.6%

Table 4b Food borne disease outbreaks by place of eating in the Republic of Korea and Japana Tableau 4b Flambees de maladies d'origine alimentaire, par lieu de consommation, en Republique de Coree et au Japona Country -Pays Rep. of Korea- Rep. de Coree Japan - Japan HomeDom1c1le Restaurant HotelHotel WorkplaceL1eu de travail SchoolEcole Retail storeMagas1n OtherDivers Unknownlnconnu

48.8% 17.2%

10.6% 32.7%

5.3% 11.5%

19.1% c. 3%

2.5% c. 4%

0.5% c. 3%

11.9% c. 16%

1.3% c. 15%

Table 4c Food borne disease outbreaks by implicated food in the Republic of Korea and Japana Tableau 4c Flambees de maladies d'origine alimentaire, par aliment incrimine, en Republique de Country -Pays Cor~e

et au Japona OtherDivers Unknownlnconnu

Seafood- Ammal products- Grain/vegetable Confectionery- Multiple foodsProduits Poissons et +mushrooms- Patisserie Aliments fruits de mer d'origine Ceniales/legumes multiples ani male +champignons

Rep. of Korea- Rep. de Coree Japan - Japan • Source: Lee

31.8% 21.7%

25.0% 3.6%

17.5% 14.6%

2.9% 1.2%

18.3% 9.6%

1.9% 1%

2.6% 48.3%

et al. (Ref. 50). - Lee et al. (Ref. 50).

the second leading cause of illnesses and death, even though these were highly underreported (53). Infected foodhandlers and pesticide residues in foods were considered to be important risk factors for foodborne disease in Vietnam, although no direct links were made between these and investigated food borne illnesses. In Thailand, the focus appears to be mainly on chemical poisonings, particularly from insecticides, although these accounted for only 0.33% of the reported 207 580 cases of foodborne disease between 1981 and 1986 (54). Between 1981 and 1987, insecticides accounted for 27.4% of outbreaks and 58.4% of cases (54, 55). Because of the widespread use of insecticides, some of these have accidentally contaminated desserts, beverages, fruits and other foods. Methomyl, which looks like sugar or flour and has little odour, was responsible for 15 of the 18 insecticide-related outbreaks. Since 1987 this chemical was sold blue-colored in an attempt to reduce these poisonings. In addition, an Wld hffh statist. quart., 50 (1997)

alcoholic beverage containing methanol affected 10 males during a party; 5 died and one had permanent visual impairment. Poisonous plants, such as mushrooms, raw cassava roots and wild plant seeds were responsible for 58.9% of outbreaks and 34% of cases, and poisonous animals, including toxins in seafood, for 11.0% of outbreaks and 6.5% of cases. There was one episode of paralytic shellfish poisoning (PSP) with 63 cases and 1 death following consumption of green mussels containing 465714 mouse units PSP toxins/ g, 4 outbreaks associated with meals made with horseshoe crab meat, and 3 outbreaks resulting from ingestion of puffer fish probably containing tetrodotoxin. The incidence of food borne disease in Malaysia was 9.62/100 000 in 1981, with the most frequent etiological agents being S. aureus, V. parahaemolyticus and Salmonella (56). In Singapore, the main bacterial pathogens isolated from 7 344 patients with diarrhoea were Salmonella (10.1 %), Campylobacter (1.2%), Shigella ( 1.1%), Vibrio parahaemolyti37

cus (0.8%) and V cholerae 01 (0.2%) (57). The sources of these were not determined but the V parahaemolyticus infections probably arose from consumption of contaminated shellfish. Pigs play an important economic and cultural role in the tribes that live in the Central Highlands of New Guinea. In the Indonesian part of the island (Irian Jaya) the prevalence of cysticerosis is the highest in the world according to Muller et al. (58), with a rate of over 30%. Pork is often consumed insufficiently cooked to destroy parasites or bacterial spores. Pig-bel, a severe form of Clostridium perjringens enteritis, is associated with ritual feasts involving consumption of roast pork in Papua New Guinea (59). There were 721 food borne outbreaks and 1 199 sporadic cases in the twin cities of Hyderabad/ Secunderabad, India, between 1984 and 1989 (60). The majority of outbreaks affected 2-10 persons, and occurred between February and June. The main vehicles of transmission were "stale" food (36.5%), rice dishes (23.5%), sweets (12.6%) and curry (9.8%). "Stale" food is probably food that has been left over from a previous meal at room temperature for a lengthy period of time, usually overnight (61). Chicken, pork, goat and fish were the most frequent components of curries and rice dishes, and were most often eaten at parties or in homes. S. aureus and Bacillus spp. were the most likely causative agents since they are often present in these foods.

Foodborne disease outbreaks A very large outbreak of hepatitis A occurred in Shanghai in January and February, 1988, with 292 301 cases and 32 deaths. The virus was transmitted through clams contaminated with sewage water (62, 63). From information available up to 1989 there were 745 outbreaks and 2 861 cases attributed to botulism in China with a 14.7% fatality rate. Most of the outbreaks (71.8%) were from home-fermented bean or cereal products (64). As more commercial products become available to the population, it is expected that fewer homemade products will be consumed and there will be correspondingly fewer botulism outbreaks. Between 1985 and 1990 in Taiwan there were 28 cases of Vibrio vulnificus infections (65). Most of these cases had ingested seafood or had exposed abraded skin to seawater. In Japan, for the most recent years, Salmonella has become much more frequent because S. enteritidis infections arising from consumption of eggs or egg products have been increasing (2). Furthermore, in 1996, there was widespread public concern after a number of large outbreaks due to E. coli 0157:H7 occurred and several children died. In July and August, in Sakai City, a total of 6 309 schoolchildren and 92 staff from 62 elementary schools were affected and a further 160 sec38

ondary infections developed, mainly in family members of the schoolchildren (66). In Habikino City another outbreak affecting 98 persons in a home for the elderly and 3 other small outbreaks in the same region occurred. All of the strains from the 5 outbreaks had identical DNA patterns, and radish sprouts from one farm were consumed by those ill. However, no isolates could be obtained from samples of soil, water and sprouts on the farm. A total of9 578 cases of E. coli 0157:H7 and H- and 11 deaths were documented from outbreaks and sporadic cases as of 26 August, 1996. No responsible foods have yet been identified, except in a few isolated cases. Tetrodotoxin puffer fish poisoning is one of the most serious in Japan; in 1982 there were 26 episodes and 8 deaths, but only 1 death in 1990 (67). In fact, the reduction in deaths has been consistent over the years from 411 in 1949 to 1 in 1990. In 1991, 21 persons in an inn near Tokyo suffered from cholera and one died after they consumed contaminated imported Korean clams (68). There had been a cholera outbreak in the Republic of Korea at that time. In Malaysia, in 1983 at a school canteen, 48 students eating meehoon (fried rice noodles) developed S. aureus intoxication. The organism was isolated from the vomitus and nasal swabs of 3 food handlers (56). The source of the S. aureus was not identified, since only scanty growth of the organism was obtained from the positive food handlers. S. aureus was also implicated in one outbreak in Hyderabad, India, when over 100 persons fell ill after eating a sweet porridge (69). About 1 000 persons suffer from foodborne disease in this city each year at an estimated cost of $10 480. As in India, sweet dishes are vehicles for S. aureus intoxication in Pakistan (70). One such outbreak from khoa, a confectionery with concentrated buffalo milk, caused 8 persons to be hospitalized in the early 1980s. More recently, some samples of khoa obtained from manufacturers in a large city contained up to 108 S. aureus/ g. Salmonella was also found in khoa and in cheese-based confectioneries (70). Pulses, ground meat dishes and chick peas vended at bus and train stations in the same city contained 104-107 C. perfringens/g, when the holding temperature was not hot enough (28-46 °C) (71). Home-prepared foods in small communities also contained pathogens, such as S. aureus, C. perjringens and B. cereus, but not Salmonella. The main hazard identified was holding foods for long periods of time, e.g., overnight, at ambient temperatures (72). An outbreak involving soy milk affected 35 of 263 schoolchildren at a midday meal in Dehli (73). The 30-minute incubation period and mild symptoms were indicative of S. aureus or B. cereus intoxication, although only E. coli at >105/ml were found in the milk.

Rapp. trimest. statist. sanit. mond., 50 (1997)

In a village in Sri Lanka the carcass of a freshlydead monkey, including its entrails, was made into a curry and 9 persons who ate this were subsequentlyinfected with S. enteritidis phage type 8 (74); one died. Other dead monkeys found later in the same area were suspected to have suffered from Salmonella septicemia, but no samples were taken for microbiological analysis. It was assumed that the curry contained Salmonella-contaminated meat and that the heat was insufficient to destroy the pathogen. In Bombay, 132 persons were ill and 4 died after eating fish that were harvested from algae-rich water and an algal toxin was believed to be responsible for their symptoms (75). Around the coastline of India, Pakistan, Myanmar and Thailand, seafood toxins such as paralytic shellfish poison (PSP), diarrhetic shellfish poison (DSP) and histamine, are a risk. However, Vibrio and Salmonella infections, through consumption of fish and crustaceans, are more frequent (75).

factors were consumption of raw or undercooked foods (especially poultry and unpasteurized dairy products) and untreated drinking water, overseas travel and contact with animals. Thorough cooking of chicken could significantly reduce the incidence of campylobacteriosis.

Foodborne disease annual reports A recent summary for the years 1980 to 1995 by Crerar et al. (79) indicates that the agents responsible for illness are similar to those in other industrialized countries with Salmonella being the predominant cause of morbidity and mortality (Table 6). However, S. enteritidis does not seem to be a major problem in Australia. Vibrio parahaemolyticus infections were greater than in North America or Europe, but this probably reflects the fact that most of Australia's population live close to the sea and consume seafood regularly. Scombrotoxin and viral outbreaks were also associated with seafood.

Oceania Epidemiological studies In Australia, some trends in notifications of enteric diseases are apparent for 1991-95 (Table 5). Laboratory isolates for Campylobacter and Salmonella isolations are increasing, those for Shigella and Yersinia are decreasing and those for Listeria monocytogenes vary slightly from year to year. New Zealand updated its notifiable diseases in 1996 to include botulism, campylobacteriosis, cryptospridiosis, giardiasis, listeriosis, toxic shellfish poisoning, VfEC, and yersiniosis (76). A surveillance of listeriosis was conducted in 1995: there were 15 cases compared with 11 in 1994 (77). Three of the cases were perinatal and 2 of the infants died. Of the remaining 12 cases, 11 had underlying disease or were elderly. None of the cases were in clusters and there were no links to food. Risk factors for campylobacteriosis were determined through a case-control study from June 1994 to February 1995 (78). The main

Foodborne disease outbreaks S. mbandaka caused at least 54 cases of illness in Victoria and South Australia in 1996 and was shown to result from consumption of one brand of peanut butter (80). Individuals infected with this rare serotype occurred in other states and territories and about half of the cases were under 5 years of age; links to peanut butter were only established in 3 Western Austalian cases. One case also occurred from the same brand of peanut butter in New Zealand. The product was recalled in both countries. Although sporadic cases of haemolytic uraemic syndrome (HUS) have been associated with E. coli 0 Ill and other VIEC in Australia, the first outbreak was in 1995 when mettwurst produced by a small manufacturer infected many people and caused HUS in 23 children with 1 death (81). This stimulated considerable interest in VfEC infections and HUS. In a study of 55 cases of Queensland children with HUS, most of those preceded by

Table 5 Notifications of selected enteric diseases in Australia, 1991-1995a Tableau 5 Cas notifies de maladies intestinales, Australie, 1991-1995a YearAnnee 1991 1992 1993 1994 1995 a Source: NatiOnal

CampylobacteriosisCampylobacteriose 8 672 9135 8 311 10 117 10 933

SalmonelloSIS Salmonellose 5 440 4 614 4 731 5 283 5 895

ShigellosisShigellose 902 894 708 724 734

ListeriOSISL1steriose 44 38 53 34 58

YerslniOSISYersiniose 515 567 450 414 306

Salmonellosis Surveillance Scheme, Communicable D1seases Intelligence Reports, Canberra, Australia.

Wld hffh statist. quart., 50 (1997)

39

Table 6 Food borne disease outbreaks in Australia, 1980-1995, by etiological agenta Tableau 6 Flambees de maladies Agent Salmonella C. perfringens S. aureus Campylobacter B. cereus V. parahaemolyticus L. monocytogenes E. coli 0111 C. botulinum Small round structured virusesPetits virus ronds structures Rotavirus Hepatitis A virus- Virus de l'hepatite A Toxoplasma Scombrotoxin - Scombrotoxine Ciguatera Mushroom poison - Champignons veneneux Total known- Total pour les agents connus Unknown - lnconnu d'o~igine

alimentaire, Australie, 1980-1995, par agent etiologiquea No. of outbreaks- %of outbreaksN de !lam bees %des !lam bees No. of casesN. de cas %of cases%des cas No. of deathsN. de deces

27 14 9 5 5 4 2

21 11 7 4 4 3 2 0.8 0.8 9 0.8 0.8 0.8 2 0.8 0.8 67 33 100

1 323 280 99 106 27 181 13 23

22 5 2 2 3 0.2 0.4 0.02 38 0.9 0.1 0.2 0.1 0.5 0.08 75 25 100

1 0 1 0 0 2 0 1 0 0 0 0 1 0 0 0 6 0 6

11

1 2 1 86 42 128

2 267 55 7 13 8 30 5 4 438 1 514 5 952

Total a Source: Crerar et al. (Ref. -Ref. 79).

diarrhoea were under 5 years of age (85%), had reduced or no urine output (71%), experienced hypertension ( 31%), and developed seizures (29%). Eighty-five percent required transfusion, 56% antihypertensive therapy, 56% peritoneal dialysis and 2% haemodialysis which lasted 3 to 29 days, and 10% ventilation (82). One child died. In February and March 1996, the first 0157 outbreak occurred in Australia when 6 persons were infected from food served in a delicatessen on the Gold Coast in south east Queensland (83). A food handler was the index case and may have contracted the infection from her pet dog which had bloody diarrhoea in the week before she developed symptoms. Recent outbreaks in New Zealand include 3 separate episodes of S. typhimurium phage type 35 associated with the consumption of bakery products in Christchurch in 1993 (84), two incidents in 1994, with people ill after eating curry probably contaminated with Clostridium peifringens, one with 31 persons at an Aukland wedding reception in March (85), and the other with 59 attendees at a fashion show in April (86), and hepatitis A in Wellington from delicatessen food contaminated by the 40

ownerI operator who was the index case in 1996 (87). The two C. perfringens outbreaks probably involved the same supplier, although this is not stated in the reports, and in one of them the practice for years had been for large pots of meat to be left at room temperature because they were too big for the cold room.

Canada and the United States Epidemiological studies In Canada, reports of enteric diseases show that campylobacteriosis is increasing, salmonellosis is decreasing, and that E. coli 0157:H7 enteritis rose to a peak after its recognition as a pathogen in 1982 and has since declined (Table 7). In the United States, salmonellosis and shigellosis appeared to be increasing from 1992 to 1995 (Table 8). E. coli 0157:H7 data are available only since 1994 with 1 420 for that year and 2 139 for 1995; despite the recent publicity on this pathogen, there are approximately 0.5 cases per 100 000 population caused by it, much less than reported in Canada (4.0 cases per 100 000). A survey of used cellulose Rapp. trimest. statist. sanit. mond., 50 (1997)

Table 7 Cases of enteric diseases in Canada, 1985-1994a Tableau 7 Cas de maladies intestinales, Canada, 1985-1994a Disease- Malad1e CampylobacteriosisCampylobacteriose Salmonellosis - Salmonellose Escherichia coli 0157:H7 enteritis Enterite a Escherichia coli 0157:H7 a Source: National

1989

1990

1991

1992

1993

1994

1995

Mean no./ 100 000 in 1995N. moyen /100 000 en 1995 35 24 4

9 653 8 762 2 432

9 081 8 742 1 585

9 786 8 984 1 565

7 666 7 265 1 521

13 669 11 767 10 499 8 057 7 441 7138 1 212 1 014 1 277

Enteric Reference Centre, Laboratory Centre for D1sease Control, Ottawa.- Centre de reference nat1onal de bacteriologie enterique, Laboratoire de lutte contre la maladie, Ottawa.

Table 8 Cases of notifiable enteric diseases in the United States of America, 1992-1995a Tableau 8 Cas de maladies intestinales adeclaration obligatoire, Etats-Unis d'Amerique, 1992-1995a Enteric disease- Malad1e intestinale Salmonellosis - Salmonellose Shigellosis - Shigellose Escherichia coli 0157:H7 enteritis Enterite a Escherichia coli 0157:H7 a Source: Summary of

1992

1993

1994

1995

40 912 23 931 not reported non rapporte 133).- Donnees

41 641 32196 not reported non rapporte

43 323 29 769 1 420 133).

45 970 32 080 2 139

not1f1able diseases (Ref.

recapitulatives sur les maladies adeclaration obllgatoire (Ref.

sponges and cotton dishcloths collected from households in 4 United States cities showed that these had a considerable faecal coliform load in liquid wrung from the sponges and dishcloths (4.5 X 102 CFU/ml and 2.0 x 103 CFU/ml, respectively). Salmonella was present in 15.4% of the sponges and 13.8% ofthe dishcloths, and S. aureus in 20.0% of the sponges and 18.6% of the dishcloths (88). These soiled cleaning materials may be an important souce of bacterial contamination in domestic kitchens. A study of 80 farm families in Ontario, Canada, found that many individuals experienced mild or subclinical immunizing VTEC infection at an early age (89). VT1 antibodies were found in 41% of persons tested. E. coli 0157:H7 and 8 other serotypes were isolated from 21 persons on 16 different farms. Four of these serotypes were isolated from cattle living on the same farms. Non-0157 verotoxin producing organisms have been shown to be pathogens, but the methodology to detect them in stools or food samples is currently limited (90). Outbreaks have not been reported from Canada, but they have from the United States, Japan, the Czech Republic, Germany, Italy, and Australia; the source of these is largely unknown but in 2 of them parsley and mettwurst were implicated. Wld hffh statist.

Foodborne disease annual summaries In both the United States and Canada, salmonellosis cases seemed to have reached a plateau of about 40 000 and 9 000 each year, respectively (2), despite the fact that S. enteritidis has become a major egg-borne pathogen in the United States over the last 15 years. Moreover, illnesses from E. coli 0157:H7 and other VTEC are being documented in outbreaks from both countries, not only from ground beef but also from vegetables, milk and apple juice. Unfortunately, foodborne disease reports at the nationallevellag behind the laboratory isolation data by several years in both countries; the last published material was for 1991/92 (91, 92). Therefore, relatively current trends may not always be apparent from a passive surveillance system which is not coordinated with laboratory analysis. This delay has been a function of low priority for foodborne disease surveillance at the responsible state/provincial and federal departments over many years. However, because of increased public health concern recently over enteric disease in both countries, sentinel sites are being established in the United States (44), and an enhanced surveillance system is being developed in Canada. In the United States, data for outbreaks between 1988 and 1992 were recently published (92). The number of outbreaks and cases had not changed sub41

quatt., 50 (1997)

stantially during this period, although there was a peak in 1990 with 528 outbreaks and 19 883 cases (Table 9). Many of these were caused by Salmonella. Other pathogens responsible for foodborne illnesses were the traditional ones: S. aureus, C. perfringens, C. botulinum, Shigella, B. cereus and hepatitis A. Few E. coli 0157 outbreaks were documented during this time period. Both ciguatera and scombroid poisonings represented the bulk of the chemical illnesses. Foodborne outbreaks in prisons were assessed in the United States from 1974 to 1991, with 88 outbreaks and 14 307 cases (93). The three main pathogens implicated were Salmonella including S. enteritidis (37%), C. perfringens (34%), and S. aureus (22%). About 50% of the outbreaks had no agent identified. Beef, poultry, meat and fish salads and Mexican foods were the main foods implicated. Improper food storage and inadequate cooking were the main factors contributing to outbreaks. Because the HIV seroprevalence in prisons is higher than average (18.9% in 1989), the risk of serious infections is high in prisoners from any source including food.

In Canada, there were in 1989, 1990 and 1991, 1 248, 1 044 and 986 outbreaks, and 6 879, 6 027 and 6 408 cases, respectively (91). The number of bacterial pathogens causing illness included Salmonella, responsible for most incidents (51 in 1989, 28 in 1990, 28 in 1991), followed by Staphylococcus aureus (21, 13, 21, respectively for the same years), Bacillus cereus (19, 15, 11), Campylobacter (13, 13, 15), E coli 0157:H7 (9, 7, 16) and Clostridium perfringens (14, 3, 1). The most dramatic decrease was for C. perfringens, down to a single case incident being reported in 1991, whereas E. coli 0157:H7 incidents rose from 7 in 1990 to 16 in 1991, although most of these were small in size. There was also one outbreak of 50 cases with 5 foods containing Salmonella heidelberg and high levels of B. cereus. Incidents caused by chemical agents were next most frequent, mainly extraneous matter, rancid compounds, and heavy metals. A few incidents of paralytic shellfish poisoning, scombroid poisoning, ciguatera poisoning and mushroom poisoning occurred during the 3-year period. One large outbreak involved uncooked wild morel mushrooms served at an hotel banquet. Meat, poultry, bakery

Table 9 Food borne disease outbreaks in the United States of America, by etiology, 1988 to 1992a Tableau 9 Flambees de maladies d'origine alimentaire, Etats-Unis d'Amerique, par etiologie, 1988 a 1992a

Etiology- Ellologie

outbreaks- casesflambees cas 94 0 8 20 6 5 4 2 0 0 12 0 3 21 8 183 268 2 987 0 245 49 3 581 51 134 109 0 0 795 0 34 79 60 8124 7 608

1988

1988

outbreaks- casesflambees cas 117 7 14 13 6 3 8 0 2 7 4 920 436 524 24 257 61 295 3 0 37 329 42 36 146 7 221 284 7 117 8 750

1989

1989

outbreaks- cases!lam bees cas 136 11 13 12 8 5 3 2 5 5 9 0 5 24 3 237 295 6 290 1 240 372 22 834 43 72 80 26 23 452 0 234 262 8 9 958 9 925

1990

1990

outbreaks- casesflambees cas 122 10 9 11 4 5 6 3 2 7 0 3 26 5 214 314 4146 1 213 331 25 112 253 93 33 6 100 114 0 73 125 34 6 658 8 218

1991

1991

outbreaks- casesflambees cas 80 12 6 4 1 3 6 3 1 8 2 834 912 206 13 4 25 138 19 2 3 419 250 2 16 3 146 261 143 63 5 033 5 982

1992

1992

Salmonella C. perfringens S. aureus C. botulinum Shigella B. cereus Campylobacter E. coli V. cholerae Other - Divers Hepatitis A - Hepatite A Norwalk-like virus Virus type Norwalk Parasitic - Parasites Seafood toxins- Toxines de poissons et fruits de mer Other chemical - Produits chimiques divers Total confirmed- Total pour les etiologies confirmees Unknown- lnconnu

5 36

Total a

451

15 732

505 15 867

532 19 883

528 14 876

407 11 015

Source: Bean et al. (Ref. 92- Ref. 92).

42

Rapp. trimest. statist. sanit. mond., 50 (1997)

products and fish/shellfish were the main foods associated with illness.

Foodborne disease outbreaks Many outbreaks are published each year for the United States, and only a few are selected here. In 1994, 593 cases of S. enteritidis were identified in Minnesota after a nationally-distributed brand of ice cream was eaten (94). Pasteurized ice cream mix had been transported in a tanker previously used to carry non-pasteurized liquid egg. If it is assumed that the ice cream was contaminated in the sample taken at the same level of 0.093 S. enteritidis PT 8/g throughout the whole load, a possible 224 000 persons in the United States could have been ill. This represents a reporting rate of 0.3% even when there was widespread publicity surrounding the event. This is about the same degree of underreporting of outbreaks estimated by Todd (95, 96), about 1 case in 350. If these data are correct, they indicate that in many outbreaks the existing local/state reporting mechanism is very limited. A commercially canned cheese used as a cheese sauce on barbecue stuffed potatoes in Georgia in 1993 caused 8 cases of type A botulism (97). The mild cases and the fact that an unusual vehicle, cheese, was implicated made the diagnosis of the disease difficult. The cheese was probably contaminated with spores after the can was opened, possibly from the potatoes. In recent years Cryptosporidium had been implicated in large waterborne outbreaks, but there have been 2 foodborne episodes that indicate the parasite may also be transmitted through faecal contamination of food. In 1993, consumers of apple juice in Maine contracted cryptosporidiosis where there was evidence that the cysts came from cattle manure contaminating the apples (98). In 1995, 15 of 26 persons attending a social function in Minnesota suffered from a Cryptosporidium infection after eating a chicken salad (99). It is probable that the host had contaminated her hands through changing a diaper from an asymptomatic child in her licensed day-care home, although she washed her hands before preparing the salad. The strongest evidence that Cyclospora may be foodborne was in 1996 when raspberries probably from Guatemala caused severe diarrhoea in more than 1 400 persons in 15 states and Ontario, Canada. Because of the lack of suitable methodology to isolate the cysts from food and its probable low infectious dose, no laboratory confirmation of the parasite in fruit has yet been made. One possible source for the Cyclospora was a pesticide spray using untreated water (Marta Ackers, Florida Centers for Disease Control, personal communication). In Ontario in 1996, roast turkey served at a church supper was implicated in an outbreak of E. coli 0157:H7 with 36 cases (14 confirmed and Wld hlth statist. quart., 50 (1997)

4 seriously ill) (100). Three of the 6 ill food preparers had 0157 in their stools. The turkeys appeared to be properly cooked and may have been contaminated during the cooling on the kitchen counter. This is one of the first VTEC outbreaks associated with a church event. Other foods implicated in VTEC infections in Ontario between 1990 and 1995 were ground beef, chicken, beef, unpasteurized milk, pork, goat, seafood, eggs and apple cider (101). Turkey, chicken and eggs are not foods traditionally associated with VTEC infections. Also in Canada, 5 separate incidents of ciguatera poisoning occurred from September 1996 to February 1997. Barracuda, Spanish mackerel and doctorfish purchased in Ontario or Quebec were implicated and leftover fish were confirmed by mouse bioassay to contain ciguatoxin or related toxins. This increase in illness may reflect a growing market for tropical fish in temperate regions. An example of an international outbreak affecting both the United States and Canada involved a kosher snack item imported from Israel into North America as well as Europe. During December 1994 and February 1995, 27 cases of S. agonawere identified in England and Wales, more than double the number for the same period the year before (102). A case-control study showed a strong association between infection with S. agona phage type 15 and consumption of a peanut-flavoured savoury snack imported from Israel. Information relayed to Israel helped identify the cause of more than 2 200 phage type 15 S. agona infections in that country during the same time period (103). The combined testing of food from the United Kingdom, the United States and Canada, where the product was imported, showed that the contaminated snacks were manufactured on at least 7 separate dates during a 5-month period, between October 1994 and February 1995. Ten cases were documented in the United States but none in Canada and in other European countries contacted through Salm-Net. Voluntary recalls were carried out to avoid further illnesses.

Central and South America Notifiable and foodborne disease reporting All Central, South American and Caribbean countries have some form of notifiable disease system. Diarrhoea! diseases are one of the main causes of death in young children, e.g., 967 deaths/lOO 000 infants < 1 year old in Nicaragua compared with 0.5 deaths in Canada, and between 4 to 7 bouts of diarrhoea are experienced each year by a child < 5 years old (104 ). The causes of these are not generally known, but amoebic dysentery, trichinosis, giardiasis, shigellosis, brucellosis, typhoid fever, E. coli and hepatitis infections are all documented from Latin America and the Caribbean, and there 43

is increasing evidence to link some of these to foods. Such is the case with cholera. This disease was first documented in Peru in 1991 with a total of 600 000 cases (105). It rapidly spread to other countries, and in 1994 caused 112 611 cases and 1 229 deaths, mainly in Peru, Brazil, El Salvador, Nicaragua, Honduras, Guatemala, Mexico, Bolivia, Ecuador, and Colombia (106). The total number of cases and deaths from 1991 to 1994 was 1 061 188 and 9 989, respectively. The source of the cholera was probably contaminated food. In 1991, V. cholerae 01 was found throughout Peru in water, sewage, finfish (skin and intestines), molluscs and plankton with counts up to 105/100 mL ( 107). The disease was spread partly through consumption of street-vended foods and beverages containing ice (108). Undercooked or raw seafood may also have been implicated as these have been associated with cholera in the past ( 109). Shellfish may be contaminated not only with local sewage, but waste water pumped from ships in harbour (110). Seafood (crab, shrimp, ceviche) was implicated in several incidents among United States travelers to Ecuador and Mexico in 1992 ( 109, 111 ). The economic loss in Peru in 1991 from lost markets and tourism, absenteeism from work, medical care and the value of lives lost due to the cholera epidemic was estimated at US$ 495.3 billion (112). In Mexico, colonization of infants by heat-labile ETEC increased 400-500% during the rainy season. There was a similar increase for children who received oat gruel, but the risk of symptomatic infection was reduced by the

ingestion of herbal tea and LT-ETEC-specific antibodies in breast milk. Also, the likelihood of noninfection increased 200% for each increment in the mother's level of education and for each previous LT-ETEC-posirive episode experienced by the child (113). Salmonella may also be an important agent in Mexico, since one study showed that even with a method of limited sensitivity, 4.5% of chocolate samples in Guadalajara tested positive ( 114). Homes were the main places where the contaminated food was acquired in Venezuela (70% outbreaks) and in Parana, Brazil (42%) (115). In Parana, the other locations of acquisition were institutions (25% ), restaurants (15%), and unknown (17%). In Cuba, S. aureus is the most frequently-occurring etiological agent, responsible for 22.6% of all, and 49.3% of known, outbreaks, followed by C. perfringens, E. coli (types not specified) Salmonella and B. cereus. The number of outbreaks caused by microorganisms and seafood toxins increased from 1985 to 1988 (104). Chemically-caused outbreaks were more sporadic in nature, but episodes of pesticide poisoning were reported each year. Beef, pork and chicken products, fish and shellfish were the main foods associated with illness. Creamfilled desserts were also implicated in S. aureus illnesses. Those ill primarily ate in school cafeterias or canteens at work. In 8 other countries, foodborne outbreaks and cases were documented, but with little information available on etiology or foods implicated. Table 10 shows the current state of knowledge for Latin America.

Table 10 Foodborne disease in 9 Central and South American countriesa Tableau 10 Maladies d'origine alimentaire dans 9 pays d'Amerique centrale et d'Amerique du Suda Country- Pays Brazil- Bresil Columbia- Colombia Dominican RepublicRepublique dominicaine El Salvador Guatemala Mexico - Mexique Venezuela Argentina - Argentine Buenos Aires Province Province de Buenos Aires YearsAnnees 1985-89 1983-88 1989-90 (6 months) - (6 mois) 1989 1987-89? 1981-90 1989 1990 1986-90 1988-90 No. of outbreaks N. de flambees 42-90/year/an No. of cases/year N. de cas/an 5 627-9 758 5 281-8 668 45 196 509 32 14 412 293 400 3 500 522 Other informationAutres renseignements 3,0-5,7% of cases hospitalized/year3,0-5,7%de cas hospitalises/an

9 363 23 14 35b

20 hospitalized - hospitalises No. of cases/outbreak= 41 (median) N. de cas/flambee= 41 (mediane)

• Source: VETA(Refs. - Ref. 104, 115). b Salmonella enteritidis only-Salmonella enteritidis uniquement.

44

Rapp. trimest. statist. sanit. mond., 50 (1997)

Foodborne disease outbreaks In Argentina, S. enteritidis(116)andE. coli0157:H7 ( 117) have been responsible for food borne illnesses. Between 1986 and April1990, 35 outbreaks of S. enteritidis affected 3 500 persons, largely through consumption of insufficiently cooked poultry and eggs used in mayonnaise. In Provincia de Buenos Aires, S. enteritidis caused 23% of the outbreaks, other bacteria 44%, chemicals 27% and unknown origin 6%. However, in Venezuela, Colombia and Brazil, S. aureus was the agent responsible for the majority of outbreaks, with incidents caused by C. perfringens, ETEC and B. cereus also documented. Bergdoll et al. (118) reported on 30 S. aureusoutbreaks from two regions of Brazil in 1988-90; cream-filled cakes, white cheese, sausage and milk were the foods implicated. Recently, an outbreak in Brazil was caused by a new form of staphylococcal enterotoxin, enterotoxin H, present in cheese (119). In a remote mountain community in Peru a health hazard analysis of foods prepared in homes was conducted and it was discovered that opportunities for foodborne disease were limited ( 120). Most foods were thoroughly cooked and eaten within a few hours. There were usually few leftovers. In Venezuela records have been kept since at least 1981 and, from that year to 1988, S. aureus caused 64.7% of outbreaks, Salmonella and B. cereus 5.9% each, and "faecal coliforms" 23.5%. Cheese was the most common vehicle of illness (35.3%), followed by cakes (23.5%), tuna (23.5%) and bologna, turkey and a maize beverage (each 5.9%). Cheese is often contaminated with S. aureus in this and other countries. Street-vended foods in the Dominican Republic had counts as high as 109 aerobic colony counts/g with holding temperatures usually <30 °C (121). Pathogens, however, were <103/g. Although street-vended food is frequently suspected as a source of foodborne outbreaks, there is rarely microbiological proof found during investigations. However, some babies in the Dominican Republic that were being treated for enteric infections came from homes where formula and other foods were prepared in a hazardous manner (122). Pathogens were found in these foods and the kitchen environment. Botulism has been reported from Argentina, Brazil, Chile, Guatemala, Peru, Mexico and Venezuela (123, 124), but incidents are not listed along with other food borne diseases (104 ). Seafood toxins are important in coastal regions. Ciguatera is a major concern in the Dominican Republic where it can affect the tourist trade as well as the residents (125, 126). There have been major outbreaks in the United States Virgin Islands, Cuba and the Dominican Republic, and fish containing ciguatoxin is an ongoing problem in many of the northern Caribbean Islands. One exceptionally large outbreak of ciguatera poisoning affected Wld hlth statist. quart., 50 (1997)

57 Canadian tourists staying in a Cuban resort (127). Paralytic shellfish poisoning has occurred in Argentina, Chile, Costa Rica, El Salvador, Guatemala, Honduras, Mexico, Nicaragua and Venezuela (128). One hundred and eighty-seven cases and 26 deaths arose from the first documented outbreak in Guatemala in 1987 when a red tide of Pyrodinium bahamense var compressa contaminated shellfish on many beaches on the coast (129). Scombroid poisoning through histamine in fish is recorded from Cuba, but must also occur in other countries. For instance, a marlin exported from Ecuador to Canada gave rise to 12 cases of histamine poisoning (130); a similar episode was documented in the United States (131). Presumably, these fish are sold locally and to other South American countries. Most Latin American countries now recognize that food borne disease is important enough to justifY some kind of surveillance scheme and are trying to develop better ways of determining numbers of cases and their causes ( 104, 115).

Conclusion This worldwide survey shows that microbiological issues are the major ones in all the countries conducting foodborne disease surveillance programmes. Salmonella, S. aureus and the better recognized agents continue to plague most countries, and E. coli 0157 and other VTEC strains, parasites, and other emerging pathogens are presenting new challenges to the food industry and national authorities. Despite our knowledge of the source of these organisms and factors contributing to disease, there seems to be little decrease in numbers affected, and the socio-economic impact of foodborne disease remains very high. One reason that control is difficult to achieve is because surveillance is inadequate and the burden of foodborne disease is not fully understood by policy-makers. Another reason is that a consistent and coordinated effort by industry and government is required. With increasing world trade and travel, improvement of surveillance on a worldwide basis is all the more important. In the United States and the United Kingdom, sentinel general practitioner studies are under way to find out the nature and causes of gastroenteritis (44). Both epidemiological and laboratory components are being incorporated into these programmes. The United States commitment to this was reinforced by the presidential proposal for the 1998 budget to allocate $43 million for a programme to detect foodborne outbreaks before they become widespread and also to reduce the estimated 6.5 million-33 million people who become ill and 9 000 who die every year from foodborne diseases (132). These initiatives should stimulate other countries to conduct appropriate surveillance programmes, so that the real burden of food borne disease can be determined at 45

various national levels. If it is now being recognized as a major concern in industrialized countries such as the United States and the United Kingdom, how much more of a problem is it in countries where urban growth is faster than the public health infrastucture can support, and in rural areas where drinking water is frequently contaminated? This issue is becoming increasingly important now that immigrants from developing countries are becoming more frequent, international travel is commonplace, and trade barriers between blocks of countries are coming down. International organizations, such as WHO and FAO need to take a lead role in accomplishing better surveillance for both industrialized and developing countries, by building on the existing expertise, and insisting on the required funding to accomplish this. Since risk assessments, used to prioritize programmes and be consistent with the World Trade Organization (WTO), are dependent on good outbreak data, food surveys, and population demographics, all countries have to be involved.

Nevertheless, data from around the world do show some common elements. Salmonella is still the most important agent causing acute food borne disease, with Salmonella enteritidis and S. typhimurium being of most concern. Foods of animal origin, particularly, meat and eggs, were most often implicated. Desserts, ice cream and confectionery items were products also mentioned, but some of these would have egg as a raw or incompletely cooked ingredient. Incidents most frequently occurred in homes or restaurants, and the main factors contributing to outbreaks were poor temperature control in preparing, cooking and storing food. Clostridium botulinum, Salmonella and VTEC are more frequently documented in industrialized than in developing countries. ETEC, EPEC, Shigella, Vibrio cholerae and parasites are the main scourges in developing countries, but it is uncertain how many cases are attributed to food, to water or to person-to-person transmission. The apparent decrease of S. aureus and C. perfringens outbreaks in industrialized countries may be related to improved temperature control in the kitchen. An increasing number of illnesses are international in scope, with contamination in a commercial product occurring in one country and affecting persons in several other countries, or tourists being infected abroad and possibly transmitting the pathogen to others at home. For Salmonella, a rapid alert and response coordination is being encouraged through Salm-Net and other international programs. However, unless such a network is worldwide, tracking clusters of illnesses is going to fall on the countries where the f1rst cases occur, and some of these have very limited resources for investigation and control. lt was heartening to see funds recently being allocated to foodborne disease surveillance and control in several industrialized countries, but the same commitment is required by the World Health Organization for the international community.

Summary Acute foodborne disease infections and intoxications are much more of a concern to governments and the food industry today than a few decades ago. Some of the factors that have led to this include the identification of new agents that have caused life-threatening conditions; the finding that traditional agents are being associated with foods that were of no concern previously; an increasing number of large outbreaks being reported; the impact of food borne d1sease on children, the aging population and the immunocomprom1sed; m1grant populations demanding their traditional foods in the countries of settlement; the ease of worldwide shipment of fresh and frozen food; and the development of new food industries, Including aquaculture. However, to meaningfully monitor increases or decreases in foodborne disease requires an effective surveillance system at the local, national and international levels. To date, resources have been limited for most countries and regions to do this, and our current knowledge is based, for the most part, on passive reporting mechanisms. Laboratory isolation data and reports of notifiable diseases have some value in observing timely changes in case numbers of some enteric diseases, but they usually do not indicate the reasons for these trends. Special epidemiological studies are useful for the area covered, but it is often questionable whether they can be extrapolated to other areas or countries. Outbreak investigations tell us that a certain set of circumstances led to illness and that another outbreak may occur under similar but not necessarily identical conditions. Control programmes have often been triggered by the conclusions from investigations of specific outbreaks. Unfortunately, the agent/ food combination leading to illness in many of the reported incidents were not predicted from existing databases, and no doubt food borne agents will continue to surprise food control agencies in the foreseeable future.

Resume Epidemiologie des maladies d'origine alimentaire: situation mondiale Les taxi-infections alimentaires aigues sont actuellement beaucoup plus preoccupantes pour les pouvoirs publics et l'1ndustrie alimentaire qu'il y a quelques decennies. Parmi les facteurs a l'origine de cette situation figurent la decouverte de nouveaux agents pathogenes provoquant des maladies parfois mortelles, !'association nouvelle d'agents traditionnels avec des aliments qui ne posaient jusqu'alors pas de problemes, le nombre croissant de flambees rapportees, l'impact des maladies d'origine alimentaire sur les enfants, les personnes ~gees et les personnes immunodeprimees, la demande, par les populations migrantes, de leurs aliments traditionnels sur leurs lieux d'etablissement, la facilite d'expedition des aliments frais et congeles, et le developpement de nouvelles industries alimentaires, comme l'aquaculture. Cependant, pour suivre valablement !'augmentation ou la diminution de ces maladies, il taut un systeme efficace de surveillance aux niveaux local, national et international. Actuellement, la plupart Rapp. trimest. statist. sanit. mond., 50 (1997)

46

des regions et des pays manquent de ressources a cette fin, et la situation est le plus souvent connue par des mecanismes de notification passifs. Les donnees des isolements realises au laboratoire et les rapports concernant les maladies a declaration obligatoire sont utiles pour suivre en temps voulu les modifications du nombre de cas de certaines maladies intestinales, mais ne donnent en general aucune indication sur les causes de ces tendances. Les etudes epidemiologiques speciales sont utiles dans la region consideree, mais leurs resultats peuvent ne pas etre extrapolables a d'autres regions ou pays. Les investigations sur les flambees nous apprennent qu'une serie de circonstances a conduit a la maladie et qu'une nouvelle flambee pourrait survenir dans des circonstances similaires ma1s non necessairement identiques. Souvent, des programmes de lutte ont ete decides au vu des conclusions d'investigations menees sur des flambees. Malheureusement, dans nombre de cas, !'association agent pathogeme/ aliment ayant conduit ala maladie n'avait pas ete prevue d'apres les bases de donnees existantes et il ne fait pas de doute que les agents de ces maladies continueront a prendre de court les organismes de contr61e des denrees alimentaires. Neanmoins, les donnees recueillies a l'echelle mondiale font ressortir certains points communs. Salmonella est toujours le plus important facteur de maladies aigues d'origine alimentaire, Salmonella enteritidis et S. typhimurium etant les especes les plus dangereuses. Les aliments d'origine animale, en particulier la viande et les ooufs, sont le plus souvent impliques. Les desserts, cremes glacees et patisseries sont egalement mentionnes, mais certains d'entre eux contiennent des ooufs crus ou incompletement cuits. Les incidents surviennent le plus frequemment en milieu familial ou dans les restaurants; le principal facteur contribuant a !'apparition de flambees est l'insuffisance du contr61e de la temperature au cours de la preparation, de la cuisson et de la conservation des aliments. Clostridium botulinum, Salmonella et Escherichia coli verotoxinogene sont plus souvent signales dans les pays industrialises que dans les pays en developpement. Dans ces dern1ers, les principaux agents en cause sont E. coli enterotoxinogene et E. coli enteropathogene, Shigella, Vibrio cholerae et les parasites, mais on ne sait pas exactement quelles sont les proportions de cas imputables aux aliments, a l'eau ou a une transmission interhumaine La diminution apparente des flambees dues a Staphylococcus aureus et a C. perfringens dans les pays Industrialises pourrait etre liee a une amelioration du contr61e de la temperature dans les cuisines. De plus en plus de maladies ont une portee internatlonale : un produit commercial peut etre contamine dans un pays et provoquer des maladies dans plus1eurs autres, ou des touristes peuvent etre infectes a l'etranger et transmettre l'agent pathogene a d'autres personnes une fois rentres chez eux. Pour Salmonella, SalmNet et d'autres programmes internationaux encouragent l'alerte rap1de et la coordination de la reponse en cas de flambee. Cependant, tant qu'un tel reseau ne sera pas mondial, le depistage des groupes de cas incombera aux pays ou surviennent les premiers cas, pays dont certains ne disposent que de moyens tres limites d'investigation et de lutte. 11 est encourageant de Wld hlth statist. quart., 50 (1997)

constater que des fonds ont recemment ete alloues a la surveillance des maladies d'origine alimentaire et a la lutte contre ces maladies dans plus1eurs pays industrialises, mais !'Organisation mondiale de la Sante aurait besoin d'un meme engagement a l'echelle de !'ensemble de la communaute internationale.

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