Measures for the control of Campylobacter spp. in chicken meat: meeting report

Measures for the control of Campylobacter spp. in chicken meat Meeting report 46 MICROBIOLOGICAL RISK ASSESSMENT SERIES ISSN 1726-5274

46 MICROBIOLOGICAL RISK ASSESSMENT SERIES Measures for the control of Campylobacter spp. in chicken meat Meeting report Food and Agriculture Organization of the United Nations World Health Organization Rome, 2024 Required citation: FAO & WHO. 2024. Measures for the control of Campylobacter spp. in chicken meat – Meeting report. Microbiological Risk Assessment Series, No. 46. Rome. https://doi.org/10.4060/cc9607en This publication contains the collective views of an international group of experts and does not necessarily represent the decisions or the policies of FAO or WHO. The expert group members alone are responsible for the views expressed in this publication and they do not necessarily represent the views, decisions or policies of the institutions with which they are affiliated. 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Cover picture cDennis Kunkel Microscopy, Inc. iContents Contributors iii Acknowledgements v Abbreviations vi Declaration of interests vii Executive summary viii Scope and objectives viii Conclusions ix Introduction 1 1.1 Request from Codex 1 1.2 Consumption and production 2 1.2.1 Global consumption of chicken meat 2 1.2.2 Intensification of broiler chicken production to meet growing needs 3 1.3 Scope of this report 3 1.4 Literature survey 4 Control measures 5 2.1. Controls during primary production 5 2.1.1. Biosecurity, management and awareness of Campylobacter prevalence addressed in approaches to control Campylobacter spp. 5 2.1.2. Vaccine- and bacteriophage-based approaches for the control of Campylobacter spp. 9 2.1.3. Feed and drinking water additives approaches for the control of Campylobacter spp. 12 2.2. Control measures during processing 16 2.2.1 Effectiveness of specific processing procedures 18 2.3. Controls during post-processing, retail and consumer levels 22 2.3.2 Effectiveness of specific retail/post-processing measures 22 Review of the Code of Practice 25 1 2 3 ii Concluding remarks 27 Intervention summary synopsis 29 References 33 Annex 55 Annex 1 The keywords used for searching the control measures of Campylobacter spp. in poultry 57 Annex 2 The questions for the two-step relevance screening and confirmation 59 A2.1. Relevance screening 59 A2.2 Relevance confirmation 60 Annex 3 Recommended revisions to the Guidelines for the Control of Campylobacter and Salmonella in Chicken Meat (GXG 78-2011), as they relate specifically to the control of Campylobacter spp. 63 Annex 4 Bibliography used for scoping review 71 A 4.1 Primary 71 A4.1.1 Biosecurity and management approaches Review of the Codex guidelines 71 A4.1.2 Vaccine and phage based approaches 77 A4.1.3 Feed and water additives approaches 80 A4.2 Processing 87 A4.3 Post-processing 105 4 5 6 7 iii Contributors Experts  Marianne Chemaly, French Agency for Food, Environmental and Occupational Health & Safety, France Frances Colles, University of Oxford, the United Kingdom of Great Britain and Northern Ireland Alessandra De Cesare, Department of Veterinary Medical Sciences, University of Bologna, Italy Moses Gathura Gichia, Food Safety Consultant, Nairobi, Kenya Ihab Habib, College of Agriculture and Veterinary Medicine, United Arab Emirates University, the United Arab Emirates Nicol Janecko, Quadram Institute Bioscience, the United Kingdom of Great Britain and Northern Ireland (served as Rapporteur) Catherine M Logue, Department of Population Health, College of Veterinary Medicine, University of Georgia, the United States of America  Marcos Sanchez-Plata, Texas Tech University, the United States of America Elina Tast-Lahti, National Veterinary Institute, Sweden  Jaap A. Wagenaar, Faculty of Veterinary Medicine, Utrecht University, the Kingdom of the Netherlands (served as Chair) Bing Wang, University of Nebraska-Lincoln, the United States of America Resource persons  Jose Emilio Esteban, Codex Committee on Food Hygiene, the United States of America  Evelyne Mbandi, Codex Committee on Food Hygiene, the United States of America Sarah Cahill, Joint FAO/WHO Food Standards Programme, Italy Jorge Pinto Ferreira, Food Systems and Food Safety Division, Food and Agriculture Organization of the United Nations, Italy  iv Secretariat  Akio Hasegawa, Department of Nutrition and Food Safety, World Health Organization, Switzerland Christine Kopko, Food Systems and Food Safety Division, Food and Agriculture Organization of the United Nations, Italy  Jeffrey LeJeune, Food Systems and Food Safety Division, Food and Agriculture Organization of the United Nations, Italy Juliana de Oliveira Mota, Department of Nutrition and Food Safety, World Health Organization, Switzerland Moez Sanaa, Department of Nutrition and Food Safety, World Health Organization, Switzerland Kang Zhou, Food Systems and Food Safety Division, Food and Agriculture Organization of the United Nations, Italy vAcknowledgements The Food and Agriculture Organization of the United Nations (FAO) and the World Health Organization (WHO) would like to express their appreciation to all those who contributed to the preparation of this report through the provision of their time and expertise, data and other relevant information before, during and after the meeting. Special appreciation is extended to all the members of the expert committee for their dedication to this project, to Jaap Wagenaar for his expert chairing of the committee, and to Nicol Janecko for her excellent support as rapporteur. All contributors are listed in the following page. Appreciation is also extended to all those who responded to the calls for data that were issued by FAO and WHO. The preparatory work and expert meeting convened to prepare this report was coordinated by the Secretariat of the Joint FAO/WHO Expert Meetings on Microbiological Risk Assessment (JEMRA). vi Abbreviations CCFH Codex Committee on Food Hygiene CFU Colony forming unit DNA deoxyribonucleic acid FAO Food and Agriculture Organization of the United Nations GHP good hygiene practices HACCP Hazard Analysis and Critical Control Points JEMRA Joint FAO/WHO Expert Meetings on Microbiological Risk Assessment QMRA quantitative microbial risk assessment WHO World Health Organization WOAH World Organisation for Animal Health vii Declaration of interests All participants completed a Declaration of Interests form in advance of the meeting. All experts were not considered by FAO and WHO to have declared any interest that may be perceived as a potential conflict with regard to the objectives of the meeting. All the declarations, together with any updates, were made known and available to all the participants at the beginning of the meeting. All the experts participated in their individual capacities and not as representatives of their countries, governments, or organizations. viii Executive summary Scope and objectives In response to a request from the 52nd Session of the Codex Committee on Food Hygiene (CCFH), the Joint FAO/WHO Expert Meeting on Microbiological Risk Assessment (JEMRA) convened a meeting in Rome, Italy from 6 to 10 February 2023, to collate and assess the most recent scientific information relevant to the control of thermotolerant Campylobacter species C. jejuni and C. coli (hereafter Campylobacter) in broiler production and chicken meat, including a review of the Codex Guidelines for the Control of Campylobacter and Salmonella in Chicken Meat (CXG 78-2011).1 The scope was focused on aspects of broiler primary production from the point of chick placement into production establishments to consumer handling. The objectives were to identify and assess control measures for Campylobacter in the broiler production chain. The expert committee reviewed the available data on Campylobacter control including scientific literature published from 2008 to October 2022 and data submitted in response to a call for data for this meeting. The experts: 1) determined the quality and quantity of evidence of control measures for Campylobacter, 2) evaluated the impact of measures to control Campylobacter in the broiler production chain, 3) determined which hazard-based interventions pertained specifically to Campylobacter and which were general to the control of foodborne pathogens in the pre- and post-harvest broiler production chain, and 4) reviewed and recommended revisions to the Guidelines for the Control of Campylobacter and Salmonella in Chicken Meat (CXG 78-2011), paragraphs 1 to 115, based on the currently available scientific evidence (Annex 3). Control measure evaluation began at the time of chick placement since there is currently no evidence that parent flocks or hatchery practices contribute to the colonization of broiler chicks. The available literature on interventions was predominantly based on laboratory and pilot studies, with few commercial scale applications; therefore, limited conclusions could be reached. The experts recommend the use of a combination of multiple interventions (multihurdle 1 FAO and WHO. 2011. Codex Guidelines for the Control of Campylobacter and Salmonella in Chicken Meat (CXG 78-2011). Rome. https://www.fao.org/fao-who-codexalimentarius/sh- proxy/de/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex %252FStandards%252FCXG%2B78-2011%252FCXG_078e.pdf ix approach) suitable to production and processing stages to lower Campylobacter contamination on chicken meat. Conclusions Several interventions were identified through primary production to post-processing stages. The expert consultation concluded the following in each stage of production: Assessment of primary production interventions for the control of Campylobacter Biosecurity and management approaches • Using strict biosecurity measures (hygienic practices and sanitation) can enhance the control of Campylobacter in broiler flocks. • Risk factors for Campylobacter contamination at primary production establishments, such as partial depopulation, litter management, down period length, proximity to other livestock and slaughter age can help guide intervention strategies. Vaccination-based approaches • Currently, there are no commercial vaccines for Campylobacter readily available for any stage of primary production, and vaccination studies were limited to C. jejuni only. • Several potential vaccine candidates are in the proof-of-concept phase but cannot be considered yet as an intervention. • Some vaccines induced a cellular or humoral response in the chicken host, but this did not always translate to reduced caecal colonization by Campylobacter in pilot studies. Bacteriophage-based approaches • There are currently no commercial products available for use in primary production. • The effects of phage therapy may be transitory and prone to resistance. Feed and water additives Organic acids • In feed, short- and medium-chain fatty acids, and in particular, caprylic acid, show promise as feed additives in reducing Campylobacter in pilot studies. x• In drinking water, organic acids reduced Campylobacter in caecal/ faecal specimens at the end of the primary production period; however, the effects were not sustained to the end of production in pilot studies. Probiotics • In feed, there is inconsistent evidence on the efficacy of probiotics as an intervention for reducing Campylobacter in broilers at primary production level. Plant-based additives • In feed, the efficacy of some plant-based molecules in in vivo pilot studies showed limited reduction of Campylobacter in caecal/faecal specimens at the end of the primary production period. Assessment of processing interventions for the control of Campylobacter • Good hygienic practices (GHP) during processing are important in minimizing Campylobacter contamination on meat. • The effectiveness of interventions during processing is dependent upon the incoming flock prevalence and concentration of Campylobacter in the gastrointestinal tract and on the bird. • The impact of processing practices can be enhanced by a combination of a multihurdle approach, processing effects, physical and/or chemical interventions. Processing effects • Logistic slaughter scheduling can reduce Campylobacter cross-contamination. • Qualitative and quantitative targets for Campylobacter may be used to optimize process control. • Scalding reduces the carcass surface concentration and prevalence of Campylobacter, The result depends on the temperature, and dilution effect. • Defeathering and evisceration may increase both prevalence and concentration of Campylobacter on carcasses. • Immersion chilling can reduce (dilute) the carcass concentration of Campylobacter; however, this is dependent on the initial Campylobacter load on the incoming birds. • In combination with processing aids, immersion chilling may reduce the carcass prevalence of Campylobacter. xi • Air chilling may reduce concentration of Campylobacter, but the efficacy of air chilling in reducing prevalence of Campylobacter when used without other processing aids is inconclusive. Physical • Irradiation is effective at eliminating Campylobacter on meat. • Freezing meat reduces the concentration of Campylobacter. • Steam, ultrasonication, high-intensity light pulse, visible light, UV-C and other technologies have shown promise either at the laboratory or pilot scale, but their impact is unknown at commercial scale. Chemical • Processing aids such as chlorine derivatives, peroxyacetic acids, and organic acids added to water used for washing and/or dipping may reduce Campylobacter on carcasses. • Some marination ingredients have shown reductions in Campylobacter on meat. Post-processing interventions for the control of Campylobacter • Thorough cooking is effective at eliminating Campylobacter on meat. • The application of GHPs is important in reducing Campylobacter on meat. • Freezing meat reduces the concentration of Campylobacter. • Some marination ingredients have shown reductions in Campylobacter on meat. Available evidence for the reduction of Campylobacter was primarily focused on C. jejuni and C. coli. Interventions aimed at foodborne pathogens such as irradiation or thorough cooking are effective in eliminating Campylobacter on meat. Hazard-based interventions, good agriculture practices and hygienic practices for the general control of foodborne pathogens may be effective for the reduction of Campylobacter. There are no interventions that specifically control Campylobacter on meat. The experts recognize further data gaps exist and that new technologies may offer promising approaches to reducing Campylobacter on chicken meat. Further global changes to the industry, the growth of global populations, climate change, and increased demand for animal protein in specific regions will guide the need for further control measure assessments.

11 Introduction 1.1 REQUEST FROM CODEX Campylobacteriosis is among the most frequently reported foodborne diseases worldwide (Havelaar et al., 2015; Tack et al., 2019). In response to the requests from Codex for scientific advice, FAO and WHO have undertaken risk assessments of foodborne pathogens in various foods since 1999 (FAO and WHO, 1999). In the past, the Joint FAO/WHO Expert Meetings on Microbiological Risk Assessment (JEMRA) have conducted risk assessments of Campylobacter spp. in broiler chickens (FAO and WHO, 2008, 2009b) and evaluated intervention measures being used in the production of chicken meat (FAO and WHO, 2009a).  In its report on the global burden of foodborne disease, the World Health Organization (WHO) estimated that in 2010 foodborne Campylobacter spp. caused more than 95 million illnesses, 21 374 deaths, and nearly 2 142 000 DALYs (Havelaar et al., 2015). While numerous potential vehicles of transmission exist, commercial chicken meat has been identified as one of the most important food transmission vehicles for Campylobacter spp. At its 52nd session in 2022, the Codex Committee on Food Hygiene (CCFH) requested that JEMRA collate relevant scientific information on Salmonella and Campylobacter in chicken meat in preparation for a potential update of the existing Guidelines for the Control of Campylobacter and Salmonella in Chicken Meat (CXG 78-2011). To meet the request of the CCFH, FAO and WHO convened this expert meeting on the pre- and postharvest control of Campylobacter spp. in broiler chicken meat from 6 to 10 February 2023 at FAO headquarters, Rome. The goal of the meeting MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT2 was to gather and evaluate recent data, evidence and scientific opinions on the topic. The output aim was to provide expert opinion on intervention strategies for the control of Campylobacter in pre- and post-production chicken meat. 1.2 CONSUMPTION AND PRODUCTION 1.2.1 Global consumption of chicken meat According to FAO, the global poultry population was 27.9 billion head in 2019, with chickens accounting for 93 percent. Poultry refers to all domesticated birds raised for meat, eggs or feathers, while chicken meat (broiler chicken) production includes species of chickens raised for meat consumption. The number of chickens worldwide has more than doubled since 1990 with poultry accounting for more than 40 percent of all meat produced for human consumption (OECD and FAO, 2021). The Agricultural Outlook 2021–2030 suggests that the global meat supply will continue to expand over the next projection period reaching 374 million tons by 2030 (OECD and FAO, 2021). The overall global expansion of meat production is driven by production in China, the Americas and Africa. China alone is expected to account for the greatest increase in meat production followed by Brazil and the United States of America. The global consumption of meat protein from any animal species is also projected to increase by 14 percent by 2030, from the 2018–2020 projections (OECD and FAO, 2021). Factors influencing meat consumption include population growth and demographics, urbanization, income, meat prices, cultural norms, environmental aspects, animal welfare and people’s personal health. Chicken meat production and availability are expected to grow by 18 percent globally due to the relative affordability for middle-income consumers. International trade has also helped improve access to chicken products worldwide and increasingly so in Asia and the Near East where demand has outpaced production (OECD and FAO, 2021). Reasons for broiler chicken production growth are multifactorial and include: 1) the short birth to slaughter time compared to other meat-producing animals, 2) the ability for lower income families to gain a higher quality of life by raising birds in small-farm holdings, and 3) the overall increase in chicken meat demand as a result of population growth and growth in income levels. As a result of the continued growth of the broiler chicken market, it is necessary to review pre- and post-production practices from hatchlings to final chicken meat products to help ensure the safety and quality of this important protein source for the world’s population. CHAPTER 1 – INTRODUCTION 3 1.2.2 Intensification of broiler chicken production to meet growing needs  In many high-income countries, broiler chicken production has been intensified by increasing farm and flock sizes, developing rapidly growing chicken breeds, creating a global supply of parental stocks, and investing in optimal feeding (Li et al., 2021; Jeni et al., 2021). Typically, commercial farms receive day-old chicks, raise them to a designated age of slaughter and transport the whole flock to an abattoir. In many low- and middle-income countries, small to medium-size enterprises, backyard farming and live-bird markets dominate domestic broiler chicken meat production (Delabouglise et al., 2019; Wong et al., 2017). Biosecurity is a challenge for the entire chicken production industry but especially so for enterprises with birds raised in backyard systems and sold at live-bird markets. These less intensive chicken production systems rarely apply strict biosecurity and good husbandry practices. When farms are transitioning to increased intensification, the education and motivation of farmers in management and biosecurity is crucial. In the commercial systems, market forces such as an increased demand for chicken meat products, demand for organically raised products, animal welfare considerations, and housing requirements all need to be taken into account when designing Campylobacter spp. control strategies. Such control strategies should be designed, implemented and monitored with consideration to specific production conditions. 1.3 SCOPE OF THIS REPORT The purpose of the experts meeting was to collect, review and discuss relevant measures for control of Campylobacter spp. in broiler chicken production, from the primary production stage to consumption. The scope of the meeting included, but was not limited to, aspects of primary broiler chicken production, processing, distribution, product handling, preparation, retail and consumption of chicken meat. Emphasis was placed on the identification and evaluation of control measures to reduce campylobacteriosis associated with consumption of chicken meat, taking into consideration the effectiveness and practicalities of measures. The objectives of this meeting were:  • To review publicly available literature and guidelines from competent authorities and industry associations (e.g. compliance guidelines, code of MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT4 practices, and so on) to assess the current state of knowledge in controlling Campylobacter spp. in chicken meat. • To review mitigation/intervention measures being used at different points along the food chain and assess their effectiveness at reducing Campylobacter spp. in chicken meat.  1.4 LITERATURE SURVEY A review of the available scientific literature targeting changes in knowledge since 2008 was used to develop a bibliography. Scientific articles were selected from two databases (Web of Science and PubMed), and as there was a need to consider studies published in languages other than English, data from member countries and expert opinions were also relied upon. The records from Web of Science (n = 2498) and PubMed (n = 1964) were added into Distiller. The function “Duplication Detection” was used by comparing the Title, Author and Abstract. A total of 915 duplicate articles were found. The “Smart Quarantine” feature in Distiller was used to remove these duplicates resulting in 3547 (2498 + 1964 – 915) publications which were used to establish the working database for the meeting. The search was carried out on 23 October 2022. The keywords used for searching the literature are detailed in Annex 1. The database was further refined using a two-step process for the relevance screening and confirmation of the 3547 articles, which were prepared in a dataset for the experts to review. The details of this procedure were presented to the experts for their further review and are included in Annex 2. The experts had a further review of these publications during the meeting, to finalize whether the literature was considered control measures or not. They provided recommendations and conclusions based on the included scientific literature as well as their expert opinions. Literature with applicability to a commercial setting was considered. The final reviewed papers, not necessarily cited, are listed in the bibliography at the end of the report.  52 Control measures 2.1 CONTROLS DURING PRIMARY PRODUCTION 2.1.1 Biosecurity, management and awareness of Campylobacter prevalence addressed in approaches to control Campylobacter spp. To complete the assessment of control measures during primary production, experts reviewed 45 papers from the literature survey (listed in Annex 4.1.1). The following sections highlight the findings. • Biosecurity Biosecurity measures appropriate for the control of Campylobacter cover multiple factors, including good production practices such as strict biosecurity and sanitation (Hansson et al., 2010; Henry et al., 2011; Jonsson et al., 2012; Hasan et al., 2020; Sandberg et al., 2017; Hertogs et al., 2021; Schweitzer et al., 2021; Golden and Mishra, 2020; Georgiev, Beauvais and Guitian, 2017). These measures remain the single most effective tool to reduce Campylobacter contamination at all stages of primary production and should form the foundation of any intervention strategy. • Management The partial depopulation (thinning) has been found to have an opposite effect with an increased risk of breaching biosecurity measures and is evidenced to be a contributing factor to Campylobacter contamination of broiler chicken flocks (Crotta, Georgiev and Guitian, 2016; EFSA, 2020; van Wagenberg et al., 2016; 6 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Smith et al., 2016; Allen et al., 2008; Higham et al., 2018; Georgiev, Beauvais and Guitian, 2017). Estimates of relative risk reductions from discontinued thinning range from 2–33 percent (Crotta, Georgiev and Guitian, 2016; Georgiev, Beauvais and Guitian, 2017; van Wagenberg et al., 2016). Alternately, adequate cleaning and disinfection practices, as well as a “resting period”, to decontaminate housing between flocks have been associated with lower Campylobacter contamination of subsequent flocks (Zbrun et al., 2021; Bailey et al., 2022; Reichelt et al., 2022; Agunos et al., 2014). • Awareness of Campylobacter prevalence in primary production Campylobacter prevalence amongst broiler flocks varies by season and is dependent on the region. Temperature and humidity in countries with both temperate and warm climates has been associated with changes in prevalence (Urdaneta et al., 2023; Guerin et al., 2008; Chowdhury et al., 2013; Iannetti et al., 2020; Sindiyo et al., 2018; Seman, Gregova and Korin, 2020; Higham et al., 2018; Wanja et al., 2022). In addition, ventilation type was associated with Campylobacter prevalence in a Spanish study (Urdaneta et al., 2023). Older birds are more likely to be infected by Campylobacter, though evidence regarding prevalence of Campylobacter amongst conventional versus organic flocks, as well as breed, flock size and stocking density was mixed (Iannetti et al., 2020; Rawson, Dawkins and Bonsall, 2019; Lassen et al., 2022; McKenna et al., 2020; Seman, Gregova and Korim, 2020; Golden and Mishra, 2020; Higham et al., 2018; Borck Høg et al., 2016; Williams et al., 2013; Russell et al., 2021; Babacan et al., 2020; Griekspoor et al., 2013; van Wagenberg et al., 2016). There is a limited number of studies investigating the effect of conventional versus extensive and antibiotic-free production systems on Campylobacter species presence, antibiotic resistance and animal welfare (Hansson et al., 2010; Iannetti et al., 2020; Babacan et al., 2020; Bailey et al., 2019; Bull et al., 2008; El-Shibiny, Connerton, P.L. and Connerton, I.F., 2005). Of those studies reviewed, five reported lower Campylobacter prevalence in flocks with higher welfare scores, amongst both conventional and extensive flocks (Bull et al., 2008; Williams et al., 2013; Colles et al., 2016; Ianetti et al., 2020; Di Marcantonio et al., 2022). Older birds raised in extensive production systems were more frequently colonized by C. coli (El-Shibiny, Connerton, P.L. and Connerton, I.F., 2005; Babacan et al., 2020). Organically raised flocks were associated with lower levels of Antimicrobial Resistance (AMR) in primary production (Luangtongkum et al., 2006; Bailey et al., 2019; Hansson et al., 2021). More research is needed to understand complex interactions between rearing system, chicken age/breed and welfare in determining Campylobacter prevalence and risk to human health (Ianetti et al., 2020; Di Marcantonio et al., 2022). CHAPTER 2 – CONTROL MEASURES 7 • Sources of Campylobacter contamination into primary production settings and management interventions The age of a broiler house, number of houses on the property, house layout including ante-room(s), water sources and drinker type, proximity to other farms, livestock and other animals were all identified as risk factors for contaminating the birds by various studies (Torralbo et al., 2014; Borck Høg et al., 2016; Torralbo et al., 2014; van Wagenberg et al., 2016; Hertogs et al., 2021). Genomic typing data indicates some Campylobacter lineages are associated with specific livestock species (including broiler chickens) and wild birds, with little overlap between the Campylobacter lineage types (Colles et al., 2008; De Haan et al., 2010; Griekspoor et al., 2013; Sheppard et al., 2010). Campylobacter prevalence in wild birds appears to be associated with feeding guild, with Campylobacter genotype overriding geographic signals (Griekspoor et al., 2013; Hald et al., 2016). Transport was assessed by a few studies. The effects of transport on Campylobacter presence in broiler flocks were mixed with no clear indication of an increase or decrease (Mendes et al., 2020; Sevilla-Navarro et al., 2020). The impact of litter type on Campylobacter colonization of broiler flocks is of interest. Some evidence suggests a high incidence of foot lesions derived from wet litter conditions, which may in turn be predictive of higher Campylobacter contamination load in the flock (Williams et al., 2013; Alpigiani et al., 2017). Litter quality is included in the internationally recognized WelfareQuality® protocol and was considered a risk factor in some of the previously mentioned studies investigating links between flock welfare and Campylobacter prevalence (Ianetti et al., 2016; Di Marcantonio et al., 2022). The practice of re-use and treatment of litter between flocks varies globally, however no recommendations for best practice can be made at the current time (Rothrock et al., 2008; Bailey et al., 2022). There was evidence from Denmark and Iceland that fly screens were associated with lower prevalence of Campylobacter in flocks if high level of biosecurity measures were already in place (Tustin et al., 2010); however, no further evidence is available since the original publication. There is sparse information regarding the role of hatcheries and breeder flocks as sources of transmission of Campylobacter to primary production flocks. Vertical transmission of Campylobacter through eggs is largely rejected by the scientific community, though there are occasional reports of Campylobacter detected in the reproductive tract of breeding birds (Battersby et al., 2016). Broiler flocks are usually colonized with different strains than the parent flock (Al Hakeem et al., 2022). Campylobacter DNA has been detected from commercial broiler 8 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT chicks less than 8 days old, suggesting that early routes of contamination might have an impact in some instances, however viable culture could not be recovered (Colles et al., 2021). Vertical transmission remains a topic of investigation for some studies (Lu et al., 2021). To date, quality evidence to support this as a transmission route is lacking. Many risk factors contribute to Campylobacter spp. colonization of broiler flocks, indicating the difficulties in maintaining effective countermeasures against its entry into the broiler environment (Natsos et al., 2020). Studies have indicated that horizontal transmission from environmental sources is the most significant cause of dissemination into primary production flocks. Newer precision based genotyping studies will continue to provide further evidence to understand and refine all forms of transmission routes. It is challenging to determine the extent of impact that farm personnel or professionals visiting farms as a control measure. One study concluded disinfection of broiler houses by unskilled personnel was a risk factor for Campylobacter colonization (Natsos et al., 2020) whereas another study found no effect on Campylobacter prevalence (Näther et al. 2009). In a UK specific study, financial incentive for farmers resulted in farmers producing a greater number of flocks with lower levels of Campylobacter contamination (Higham et al., 2018). In a US-based questionnaire study of broiler industry stakeholders, it was concluded that many survey participants were unfamiliar with Campylobacter specific risk factors (Hwang and Singer, 2020). Without further assessment, the impact of personnel on the introduction and levels of Campylobacter contamination is inconclusive. Conclusions Strict biosecurity and sanitation measures are a key requirement by which to control Campylobacter and should form the foundation for any on-farm based interventions. There is some evidence that management practices can influence Campylobacter population; however, other impact factors such as seasonal Campylobacter population variation in specific geographical regions, breed of birds, and age of birds at slaughter cannot be easily controlled by management practices alone. Transmission route analyses will be helped by tools such as rapid molecular assays and genomic sequencing that will in turn contribute evidence used to guide future intervention recommendations and refinement of biosecurity measures. The genomic profiling of Campylobacter strain lineages in broiler chicken production will also enable assessment of impact when studying interactions between the chickens and environmental microbiomes. Important considerations for on-farm assessments include: CHAPTER 2 – CONTROL MEASURES 9 • whether it is necessary to partially depopulate (“thin”) flocks; • down time between flocks; • litter management and welfare of flocks; • housing, including age/ability to disinfect, ventilation and layout (ante-room[s]); and • training and compliance of staff and visitors on strict biosecurity measures. 2.1.2 Vaccine- and bacteriophage-based approaches for the control of Campylobacter spp. Vaccines are agents or portions of a bacterial cell that are used to prevent Campylobacter colonization in broiler birds and to decrease the potential for Campylobacter transmission to meat products. Vaccines against Campylobacter have been investigated over many years. A number of different vaccine types that have been investigated include attenuated, subunit, inactivated, conjugate, DNA, vector and recombinant vaccines. While efforts in developing effective Campylobacter vaccines have been made, there is currently no single vaccine approved for use in broiler bird production. Bacteriophages, the viruses that specifically infect target bacteria, thereby killing the host bacterial cell, have also been investigated for their potential to control Campylobacter. The field of Campylobacter specific bacteriophages (phages) is relatively limited with very few published data available. 2.1.2.1 Vaccination-based approaches to control Campylobacter The experts reviewed 23 papers related to vaccine studies for Campylobacter control with 14 directly applicable to the current review (Annex 4.1.2). The following sections highlight evidence pertaining to vaccination as an approach to Campylobacter control in broiler birds. • Quality of evidence Currently, there are no commercial vaccines for Campylobacter readily available. Potential candidates (e.g. reverse vaccinology approach) are on the horizon; however, most trials at present are in a “proof-of-concept phase” or have reported findings from laboratory or pilot-scale level studies. The quality of the papers was satisfactory in terms of methodology and study design that incorporate controls and challenge groups. Assessed trial studies also had a satisfactory level of statistical analysis to determine measurable effects. A range of vaccine methods and types (glycans, inserted proteins, flagellin, subunit, in ovo, and live attenuated) were included in the literature assessed (Layton et al., 2011; Jeon et al., 2022; 10 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Gloanec et al., 2022). Some approaches included an alternative vector expressing Campylobacter proteins to deliver antigens to the poultry host, e.g. Salmonella (Buckley et al., 2010; Sahin et al., 2015) and Eimeria (Clark et al., 2012), yet conclusions could not be reached on the approaches as control measures. The literature reviewed was in the proof-of-concept stage, with no papers indicating any commercial-level trials or follow-up studies, demonstrating the infancy of the field of vaccine development for Campylobacter control in broilers. • The measure of effectiveness The measure of effectiveness to control Campylobacter was reported as log level reductions in the ceca or gut (quantitative) or number of birds positive following vaccination and challenge (prevalence). Reported vaccine effects varied from no reductions of Campylobacter noted (Meunier et al., 2018; Mauri et al., 2021; Vandeputte et al., 2019) to low level reductions of 1–2 logs or less (Łaniewski et al., 2014; Buckley et al., 2010; Chintoan-Uta, Cassady-Cain and Stevens, 2016; Gloanec et al., 2022), while a few studies reported high level reductions (up to 4 logs) (Layton et al., 2011; Cui et al. 2022; Nothaft et al., 2021). There was evidence that some of the candidate vaccines appear to be promising; however, further research is warranted to examine the candidates on a larger scale, e.g. commercial farms (Cui et al. 2022; Layton et al., 2011). There is also limited evidence as to the practicality of vaccine production for these candidates on a larger scale or as to wider industry vaccination strategy. Some candidate vaccines were found to induce cellular or humoral response in the chicken host, meaning that the host immune response recognized Campylobacter, but in terms of elimination of Campylobacter from the chicken host this did not translate to stable (rather than transient) caecal colonization or reductions levels (> 2 logs) (Radomska et al., 2016; Cui et al. 2022; Gloanec et al., 2022), suggesting that the effects were not consistent and unlikely to be permanent. Most studies assessed used a homologous challenge approach (i.e. single strain, typically a C. jejuni) with no studies using a heterologous challenge (i.e. using diverse Campylobacter strains). No studies to date investigated the ability of a vaccine candidate to provide cross protection against diverse Campylobacter species. Additional studies are warranted to understand the levels and types of cross protection provided by potential vaccine candidates. • Scalability or applicability (practicability) Further studies are required for extensive scale application of candidate vaccines, i.e. farm-level production. All studies reviewed were currently at the lab or pilot-scale CHAPTER 2 – CONTROL MEASURES 11 (research farm) level only with no indication for larger pilot-scale studies such as commercial farm or production-level studies and no indication of commercial vaccine trials. Such large-scale trials will be necessary to assess the scalability and potential impact of candidate vaccines for full implementation in broiler production. • Geographical representation of the studies All vaccine candidate studies were conducted only in high-income countries or regions of the world; therefore, the translation of these studies to underdeveloped regions will warrant additional studies in specific regions to assess efficacy and practicality. Conclusion Vaccines for Campylobacter control continues to be an emerging field and warrants further investigation and investment to take proof-of-concept studies to commercial trial phases. 2.1.2.2 Bacteriophage-based approaches for the control of Campylobacter spp. The experts reviewed ten papers (Annex 4.1.2) on the use of bacteriophages as an intervention measure for Campylobacter colonization in broilers. • Quality of evidence There are currently no commercial products available for use in primary production. The bacteriophages used in the studies reviewed varied among studies, with some well-characterized bacteriophages. Of the six experimental studies reviewed, all had treatment groups and control groups, allowing assessment of the effect of phage treatment in a statistically sound manner. • The measure of effectiveness Some studies used a single phage strain (Fischer et al., 2013; Furuta et al., 2017; El-Shibiny et al., 2009), whereas others used multiple (a cocktail of ) phage strains (Carvalho et al., 2010; Kittler et al., 2013; Richards, Connerton, P.L. and Connerton, I.F., 2019; Hammerl et al., 2014; D’Angelantonio et al., 2021; Chinivasagam et al., 2020). Treatment was typically via drinking water or gavage. The effects of phage treatment on reductions of Campylobacter ranged from a 1 log to a > 3 log reduction of Campylobacter colonization in faecal droppings or caecal contents after necropsy. The effect was most evident a few days post treatment; however, Campylobacter colonization levels increased over time post treatment. In some studies, Campylobacter strains were screened for resistance to phages after treatment. Resistance was reported; however, these strains did not 12 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT overgrow susceptible strains. In some studies, there was considerable variation between groups/barns used in the study. A reduction of 3 log is considered relevant for public health, based on a risk assessment by Rosenquist et al. (2003). Over the last decade or more, there has not appeared to be any technical progress in the experimental approaches used for the application of phages for Campylobacter control. Studies do not address the variability between Campylobacter strains and the applicability or practicality of phages for field or commercial purposes. • Scalability or applicability (practicality) and geographical representation studies Except for two studies performed on-farm (Australia and Germany) (Chinivasagam et al., 2020; Kittler et al., 2013) with naturally colonized flocks, studies were performed in experimental, controlled settings. Applicability could therefore not be assessed for commercial settings. One field study was conducted in Australia (Chinivasagam et al., 2020); all other studies were performed in Europe, and therefore there is no indication of how bacteriophage approaches would be applicable in other regions. Phages are variable depending on the strain type and vary in the level of activity. Additionally, the potential for Campylobacter to develop resistance to the phage is considerable. Bacteriophage approaches to control Campylobacter are not clear. In conclusion, no recommendation on the use of bacteriophages can be made at this time. 2.1.3 Feed and drinking water additives approaches for the control of Campylobacter spp. Feed and water additives are chemical or biological supplements that can be added to water or feed formulations. Additives as a control measure of Campylobacter have been assessed for effectiveness and scalability. In-feed and in-water additives applied at the primary stage of production (farms) were reviewed. • Quality of evidence The experts reviewed a total of 89 papers by first screening and then further subdividing them into relevant subheadings of organic acids, probiotics and plant-based additives. The quality of evidence varied with most of the available literature containing laboratory and pilot stage studies. Although some studies have provided promising results as to the effects of organic acid additives, extrapolation of the evidence to the commercial scale of production systems could not readily be made. CHAPTER 2 – CONTROL MEASURES 13 • Organic acids: measure of effectiveness Seven papers reported on the impacts of medium chain fatty acids (caprylic acid) supplementation in feed. The supplementation of medium chain fatty acids in feed is considered a promising tool for the reduction of Campylobacter colonization in commercial broiler flocks (Van Gerwe et al., 2010). Therapeutic supplementation of caprylic acid at 0.7 percent in the feed for 3 or 7 days before slaughter showed a consistent 3 to 4 log reduction in caecal C. jejuni counts in market-aged broiler chickens (De Los Santos et al., 2010). The results of this study indicate that caprylic acid’s ability to reduce Campylobacter does not appear to be due to changes in caecal microflora or a decrease in intestinal pH. It is hypothesized that caprylic acid may compromise the outer membrane determinants in Campylobacter which are needed for bacterial adaptation to host environment and colonization. It is also possible that caprylic acid has a direct inhibitory effect on the expression of virulence factors necessary for C. jejuni colonization in chicks. The in-water supplementation of caprylic acid at various concentration levels did not reduce Campylobacter shedding due to the changes in adsorption and caprylic concentrations reaching the lower intestinal tract (Metcalf et al., 2011). The addition of sorbic acid, benzoic acid, propionic acid, and acetic acid in drinking water reduced the Campylobacter shedding reaching a maximum 2 log reduction during the rearing period (Gharib Naseri, Rahimi and Khaki, 2012); however, the drinking water additive failed to diminish Campylobacter colonization in the intestinal colonic and caecal contents at the time of slaughter (Szott et al., 2022). Therefore, the benefits of drinking water treatment to controlling Campylobacter shedding and transmission was not significantly evidenced and would need further investigation. Other organic acid and medium chain fatty acids showed in vitro study reductions (Greene et al., 2022); however, the efficacy in in vivo pilot and commercial scale studies were not performed, as there were negative bird performance effects in treatment groups. Ferric tyrosine added to the feed at 0.02, 0.05 and 0.20 g/kg can reduce Campylobacter in the ceca at 42 days up to 3 log (Currie et al., 2018), but other studies showed lower reductions (i.e. 2 log reduction) (Khattak et al., 2018). • Probiotics: measure of effectiveness The use of in-feed probiotic additives as a measure to control Campylobacter in birds at the primary production level was addressed in 19 papers assessed by the experts. Probiotic bacteria are thought to reduce pathogenic bacteria (including Campylobacter) in the gut through competition for shared attachment sites in the mucosa (Lu and Walker, 2001) or through production of antimicrobial 14 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT metabolites (Oelschlaeger, 2010; Neal-McKinney et al., 2012). The overall lasting reduction effect by probiotic treatment on Campylobacter presence was inconsistent across the literature. Administration of feed additives at specific stages of growth demonstrated some reduction of Campylobacter presence at midgrowth stage (day 18–21) (Ghareeb et al., 2012); however, those reductions were not sustained to the end of production. Some pilot studies demonstrated that administration of Lactobacillus casei overexpresses myosin-cross-reactive antigen (LC) in the feed and reduced C. jejuni colonization in the cecum, ileum and jejunum, by more than 1 log CFU/g when compared to the no-probiotic control group (Tabashsum et al., 2020). The strain was able to generate bioactive compounds including conjugated linoleic acid. Commercial or large-scale trials would be required to demonstrate applicability to large-scale farming. The literature predominantly reported on C. jejuni strains. Probiotic administration did not demonstrate an effect in reducing C. coli levels in caeca (Mortada et al., 2020). • Plant-based additives: measures of effectiveness Plant-based molecules added to feed and water vary in type, concentration of administration and timing of administration. Twenty-five papers addressed plant-based additives as a strategy for reducing Campylobacter within the lower gut of birds. Molecules such as trans-cinnamaldehyde, eugenol, carvacrol, and thymol demonstrated Campylobacter reduction of up to 4 logs in vitro (Kollanoor Johny et al., 2010) but to a lower extent (approximately a 2 log reduction) in vivo (Allaoua et al., 2022). In addition, other plant-molecules, such as glycyrrhiza glabra (licorice) extract, beta-resorcylic acid, and thymol were tested in pilot in vivo studies, showing limited efficacy in the reduction of Campylobacter in caecal/faecal counts (~1–2 log reduction) (Wagle et al., 2017; Ibrahim et al., 2020; Epps et al. 2015). • Other additives and combination of additives: measure of effectiveness In papers applying multiple strategies, it is difficult to assess the specific impact of individual components, and the overall effect cannot be attributed to the administration of an additive molecule. For example, up to 1 log CFU/g fewer Campylobacter were recovered from broilers administered either direct-fed Bacillus culture, prebiotic, refined functional carbohydrates (including mannooligosaccharides (MOS), b-glucans, and mannose), or symbiotic when compared to the untreated control group (Froebel et al., 2020). Refined functional carbohydrates, including MOS, b-glucans and mannose, are important to the pathogen inhibiting functionality of prebiotics (Oyofo et al., 1989; Spring et al., 2000). These carbohydrates are thought to bind to bacterial surface adhesins thereby inactivating the bacteria’s ability to infect the host (Fernandez et al., 2002; Walker et al., 2018). CHAPTER 2 – CONTROL MEASURES 15 Furthermore, the reported reduction effect of Campylobacter using a combination of in-feed additives (microencapsulated propionic, sorbic acids and pure botanicals) at different concentrations administered at various stages of growth resulted in a synergistic action between organic acids and pure botanicals (Grilli et al., 2013). Greene et al. (2022) reported the anti-Campylobacter properties of nine compounds belonging to organic acids, medium chain fatty acids and essential oils in in vitro experiments; however, it was concluded that while the tested compounds are effective against Campylobacter in laboratory model studies, the negative effects on broiler performance metrics deem the approach ineligible for use in vivo. Further large-scale in vivo studies are required to adequately evaluate the efficacy of a multi-additive approach to reducing Campylobacter in the lower gut of birds at the end stage of primary production. The field of other natural additives is expanding, and further work is required to evaluate the impacts on Campylobacter reduction in experimental, pilot and large-scale commercial trials. Other additive candidates include whey powder, which when applied in feed, may affect the physico-chemical integrity of intestinal digesta and improve the balance of intestinal microbiota (Tsiouris et al., 2020; Wilson et al., 2018) However, the existing evidence showed that the effect on the reduction of Campylobacter in caecal contents was limited based on studies conducted under both experimental and field settings. • Scalability, applicability, and geographical representation The scalability and applicability of in-feed and in-water additives is limited at this time. Smaller scale in vivo studies were conducted in some investigations; however, large-scale commercial-level studies are required to assess the efficacy of interventions at scale. Primary-source pilot studies were predominantly conducted in one region. Multiregional and commercial-scale studies were not identified in the assessed literature, limiting extrapolation of findings beyond the pilot study site. Conclusions The evidence for clear reductions to Campylobacter colonization in the lower gut of birds at various stages of primary production was inconsistent. The use of caprylic acid (in-feed) demonstrated promise in pilot studies, yet further commercial-scale evaluation is needed to assess broad-scale application. With the evidence available, probiotic and plant-based in-feed additives showed limited and inconsistent reductions to Campylobacter in pilot studies. To fully assess additives as an intervention strategy at the primary production 16 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT stage, important considerations for assessment are: • fully addressing the start and end of the additive administration and timing of measured reduction levels; • addressing whether measured reductions are calculated on naturally contaminated birds or challenged birds; and • compulsorily measuring intervention impact at the end of the rearing cycle in commercial scale conditions to appropriately assess the true reduction of Campylobacter. 2.2 CONTROL MEASURES DURING PROCESSING Experts reviewed 141 papers from the literature survey related to Campylobacter control during broiler processing. These papers include both primary studies and systematic reviews, listed in Annex 4.2. In addition to control measures developed for the primary production stage, a range of processing steps and interventions during the primary and secondary processing stages have been developed to reduce Campylobacter contamination on/in broiler chicken carcasses and parts. Such intervention measures include general hygienic improvements, technological advancement in processing operations, and decontamination strategies applied throughout or at specific processing steps. In this section, the effectiveness of different processing steps and interventions to reduce the prevalence and/or concentration of Campylobacter were critically reviewed considering the quality of evidence, practicability of the evaluated measures, and the geographical representation. • Effectiveness of good hygiene practices Good hygienic practices (GHP) are important in minimizing Campylobacter contamination during processing. Once Campylobacter is introduced in the slaughter line, it can spread to the chicken meat, especially at the defeathering and evisceration steps (Cools et al., 2005). Some Campylobacter strains may also survive after cleaning and disinfection in a slaughter environment, thus persisting longer and becoming a source of cross-contamination over time (García-Sánchez et al., 2017). The implementation and compliance of GHPs as well as following Hazard Analysis and Critical Control Points (HACCP) principles at the processing establishment is a systematic way to maintain cleanliness, control the presence and levels of Campylobacter, and minimize contamination during chicken processing. The rigorous implementation of systematic approaches can significantly enhance the integrity and wholesomeness of a food safety management system in broiler CHAPTER 2 – CONTROL MEASURES 17 processing, thereby leading to the reduction of Campylobacter contamination in broiler chicken products and a subsequent decrease in associated public health risks linked to chicken consumption (EFSA Panel on Biological Hazards, 2011). The effectiveness of good hygiene practices at the processing establishment is in part dependent upon incoming flock prevalence and concentration of Campylobacter in the gastrointestinal tract and on the bird. Elevated levels of Campylobacter on the exterior and within the intestinal contents of broilers can exert greater pressure on a good hygiene management system. A study investigating risk factors for Campylobacter contamination on broiler carcasses after slaughter found a significant correlation between the presence and quantity of Campylobacter in caecal contents and on birds arriving at the processing establishment (Hue et al., 2010). Similar finding was evidenced in an EU-wide baseline survey of Campylobacter on broiler carcasses, revealing an approximately thirtyfold increase in the probability of obtaining a Campylobacter-positive carcass post slaughter from a batch of live birds colonized with the pathogen (EFSA, 2010). Good hygiene practices alone during slaughter and processing will have limited impact on reduction levels if incoming bird contamination is high. • Effectiveness of a multihurdle approach Employing a combination of processing effects that include physical and/ or chemical interventions can enhance the impact of Campylobacter control measures. It is common to employ a multihurdle approach for a synergistic reduction of Campylobacter contamination in chicken processing. For example, processing steps such as scalding and chilling of carcasses have been shown to decrease the number of Campylobacter (Rasschaert et al., 2020). In some countries, decontaminants, such as chlorine, added to the chilling water also effectively reduce the total bacterial load on carcasses (Bucher et al., 2015). Furthermore, following an implementation of crust freezing combined with logistic slaughter, a lower prevalence was observed in fresh, chilled broiler meat in Denmark. Recently published research has evaluated the cumulative effect of combining two or more chemical and/or physical interventions in a risk assessment, which revealed that the multihurdle approach can advance the control of Campylobacter contamination in chicken products (Dogan et al., 2019). Additionally, alternative approaches in processing were evaluated. The ultrasonication of chicken drumsticks was more effective in combination with chemical processing aids, compared to chemical treatments used on their own (Koolman et al., 2014a; 2014b), or in combination with a vacuum and a water resonance system (Vetchapitak et al., 2020). Greater effectiveness was not guaranteed with the use of crust freezing and UV in combination, giving no additional benefit over the use of crust freezing alone (Haughton et al., 2012). Some may not yet be practical in a commercial plant or when used alone 18 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT (Gunther, Phillips and Sommers, 2016; Isohanni and Lyhs, 2009). 2.2.1 Effectiveness of specific processing procedures • Logistic slaughter Logistic slaughter employs a method of scheduling known colonized flocks to be slaughtered only after non-colonized flocks, at the end of a slaughter day or week. Logistic slaughter can reduce Campylobacter cross-contamination between flocks through the exposure to contaminated equipment (e.g. processing lines), as evidenced by a study where fewer positive samples were recovered from birds slaughtered after Campylobacter negative flocks compared to Campylobacter positive flocks (Reich et al., 2008). Norway, Iceland and Denmark have fully implemented logistic slaughter in national Campylobacter control programmes (Rosenquist et al., 2009). However, the impact of logistic slaughter on reducing the risk of Campylobacter infections in humans has not been fully evaluated (Nauta et al., 2009). • Qualitative and quantitative target incentives Setting qualitative and quantitative targets for Campylobacter at the processing plant may be used to optimize process control. Setting quantitative limits (e.g. Campylobacter colonies per gram of fresh meat) could provide incentive to reduce the occurrence of highly contaminated carcasses. In New Zealand, setting a quantitative regulatory limit for chilled chicken carcasses was introduced to reduce Campylobacter levels in processed chicken. This measure was also used to evaluate the effectiveness of implemented processing measures on reduction levels of Campylobacter (Wagenaar, French and Havelaar, 2013). These practices are further supported by a risk assessment of Campylobacter in chicken. Reducing the levels of Campylobacter on meat prior to reaching the consumer would be effective in reducing campylobacteriosis incidence (Nauta et al., 2009). • Scalding Reduction in Campylobacter contamination on chicken carcasses can occur at the scalding step through physical removal and cell inactivation under elevated temperatures (hard scalding). Based on a recent systematic review and meta-analysis, hard scalding with higher temperature exerts a consistent log reduction (mean: 1.85 log CFU, 95 percent CI [1.60, 2.09]) (Dogan et al., 2022), while soft scalding with lower temperature was associated with a lower log reduction. Decreased prevalence of Campylobacter on broiler carcasses associated with scalding has been consistently observed (OR: 0.18, 95 percent CI [0.11, 0.30]). Furthermore, a multihurdle approach of scalding, and using chemical additives, such as chloride, CHAPTER 2 – CONTROL MEASURES 19 had a greater reduction in both concentration and prevalence at the end of this processing step (Berrang and Dickens, 2000; Berrang et al., 2003; Berrang, Windham and Meinersmann, 2011). These findings were primarily based on studies measuring the naturally occurring contamination of Campylobacter before and after the scalding step in the pilot or processing scale. • Defeathering and evisceration The defeathering and evisceration steps during processing are associated with an increased prevalence and concentration of carcass Campylobacter contamination, implying these are critical points in broiler processing for Campylobacter contamination of downstream products (Dogan et al., 2022; Gruntar et al., 2015; Zweifel, Althaus and Stephan, 2015; Huang et al., 2017; Reich et al., 2008; Gichure et al., 2022). The increase in carcass contamination after evisceration is due to the leakage of faecal contents from pressure applied onto carcasses and visceral rupture. Primary studies suggest an overall increase in Campylobacter concentration (mean: 0.88 log CFU, 95 percent CI [0.54, 1.23]) and prevalence (OR: 5.8, 95 percent CI [1.15, 29.42]) following the defeathering step, with similar increases observed after evisceration. However, variation was observed between individual studies. The variation may be related to differences in initial contamination levels and procedural differences between processing establishment (Luning et al., 2011; Zweifel, Althaus and Stephan, 2015; Pacholewicz et al., 2016). Interventions such as organic acid injection into the cloaca and cloacal plugging have been tested and seem to be promising approaches (Berrang et al., 2001; Berrang, Smith and Hinton 2006a, 2006b; Berrang, Windham and Meinersmann, 2011). However, the feasibility of their applications on a broader scale for the industry is uncertain. • Chilling during processing During immersion chilling, broiler carcasses are dipped into cold water with or without aids to cool down processed carcasses as rapidly as possible, thereby minimizing microbial growth in the cold-water bath. The reports on the effect of immersion chilling on Campylobacter contamination of carcasses vary. In some studies, a decrease in Campylobacter concentration was consistently observed regardless of the use of processing aids to cool the carcasses (0.70–4.12 log CFU) (Dogan et al., 2022). Immersion chilling without chemical additives decreased Campylobacter 1.25 log CFU (95 percent CI [0.96, 1.55]) – a mean of 1.95 log CFU, (95 percent CI [1.46, 2.45]) when the chemical additive chloride was added, indicating that the addition of chlorine may control the concentration of Campylobacter on carcasses post chilling more effectively. Other studies report the opposite effect of immersion chilling without chemical aids with an increase 20 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT in prevalence observed (OR: 1.55, 95 percent CI [0.81, 2.96]) (Dogan et al., 2022). The increased prevalence may be explained by a cross-contamination effect of dipping carcasses into contaminated chilling water. Still, immersion chilling with chemical additives may compensate for the water contamination effect and minimally reduced prevalence (OR: 0.71, 95 percent CI [0.28, 0.61]) (Dogan et al., 2022). Adding chemical processing aids to chilling water can control the transmission of Campylobacter across carcasses during the immersion chilling process. As an alternative approach, air chilling presents some advantages over immersion chilling in product quality, thus gaining popularity in broiler processing. In terms of Campylobacter control, most studies reported a slight decrease in Campylobacter concentration associated with air chilling, showing a mean log reduction of 1 log CFU based on studies conducted at pilot or processing scale. However, most studies reported no significant effect based on studies evaluating challenged or naturally occurring contamination at either pilot or processing scale (Dogan et al., 2022). As with control measures to reduce Campylobacter during chilling, immersion chilling is more effective than air chilling in terms of reducing the exterior surface concentration of Campylobacter on broiler chicken, regardless of the use of processing aids. • Alternative Campylobacter reduction approaches Freezing and ionizing (gamma) irradiation have been shown to be effective in reducing Campylobacter contamination on chicken carcasses but are not recommended as the primary method of pathogen control (Umaraw et al., 2017; Gellynck et al., 2008; Gunther et al., 2019; Cox and Pavic, 2010). Experimental trials have shown that crust freezing of chicken meat portions may reduce Campylobacter by up to 1.5 log CFU with minimal impact on the colour of treated skin (Haughton et al., 2012). In addition, flesh temperature may be maintained above – 2 °C (Burfoot et al., 2016) consistent with the EU target for selling fresh, rather than frozen, meat. Steam, ultrasonication, high-intensity light pulse, visible light, and UV-C among others have shown promise either at the laboratory or pilot scale, but their impact is unknown at commercial scale (Sorro et al., 2020; Chun et al., 2010; Koolman et al., 2014a, 2014b; Vetchapitak et al., 2020; Haughton et al., 2012; Moazzami, Fernström and Hansson, 2021). CHAPTER 2 – CONTROL MEASURES 21 • Chemical additives as a Campylobacter reduction approach In the countries and regions where chemical processing aids are permitted for use in chicken processing, common examples include chlorine, chlorine derivatives (e.g. chlorine dioxide, acidified sodium chlorite), peroxyacetic acids (PAA), organic acids (e.g. lactic acid [LA]), and quaternary ammonium compound (e.g. cetylpyridinium chloride [CPC]) (Ebel, Williams and Tameru, 2019). These chemical aids are added to water used for spray and/or immersion, with the aim of reducing Campylobacter on broiler carcasses and parts. Studies have documented variation in the effectiveness of chemical processing aids, reporting factors such as initial contamination, amount of organic matter on the bird and carcass and chemical application conditions responsible for variation in Campylobacter reduction levels. Among the different classes of chemical processing aids, chlorine may be less effective as an intervention in decontaminating carcasses containing Campylobacter in comparison to PAA, during the pre-chill, chill or post-chill immersion or spray application step (Cano, Meneses and Chaves, 2021). Organic acid such as lactic acid is a chemical control option considered during post-chill treatments, as it has fewer occupational concerns. Peroxyacetic acids and lactic acid demonstrate comparable reduction levels in Campylobacter contamination in immersion studies, while the comparison for spray applications is inconclusive. Effectiveness of PAA was comparable to or higher than that of CPC, depending on specific product type and treatment conditions (Cano, Meneses and Chaves, 2021; Dogan et al., 2022). Unlike physical processing effects, the effectiveness of chemical processing aids has mostly been investigated in challenge studies conducted in laboratory settings or pilot plants, which may introduce uncertainty when extrapolating the impact of such aids on naturally occurring contamination at a broader processing scale. Marinades are commonly used to enhance the sensory characteristics of meat, yet studies have also demonstrated their potential to reduce Campylobacter on chicken meat. Marinades typically contain water, salt, spices, sugar, wine, and acidic ingredients like vinegar, lemon, or lime juice (Lopes, Da Silva and Tondo, 2022). The use of marinades for chicken cuts such as breast, fillets and wings reduced Campylobacter contamination from 0.5 to 3 log CFU (Park, Hong and Yoon, 2014; Birk et al., 2010; Zakarienė et al., 2015; Isohanni et al., 2010), with some studies reporting reductions of up to 6 log CFU (Thanissery and Smith, 2014). pH was identified as the most significant factor influencing Campylobacter inactivation, although other factors such as specific ingredients’ compounds and storage temperature also played a role. Currently available evidence was collected from studies conducted in laboratory settings using inoculated chicken cuts and parts. 22 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT 2.3 CONTROLS DURING POST-PROCESSING, RETAIL AND CONSUMER LEVELS The experts reviewed 77 papers, of which 19 were strictly related to post-processing stages of chicken meat production. Control measures were evaluated and highlighted in the next section (Annex 4.3). 2.3.2 Effectiveness of specific retail/post-processing measures • Freezing of meat product Laboratory-based studies found that freezing chicken meat for 1 week at 20 °C significantly decreased Campylobacter counts on meat by 1.73 log CFU/g (Bolton et al., 2014). Continued storage resulted in additional reductions, but the greatest reductions occurred after the first week. Other studies have also reported freezing at – 20 °C resulting in reductions of 2.2–2.6 logs within 9 days of storage (El-Shibiny, Connerton, P. and Connerton, I., 2009). Variability was noted in the survival of strains examined, suggesting that Campylobacter strains have varying levels of freezing resistance. Where studies of contaminated cooked product were undertaken, low level contamination (50 CFU/g) could not be detected on 70 percent of frozen samples after storage for 7 days and was detectable at reduced levels on 92.5 percent of samples inoculated with 500 CFU/g, suggesting that the organism can survive freezing (Eideh and AlQadiri, 2011), posing a potential health risk where cross-contamination of cooked product occurs. Freezing is an effective control measure for reducing Campylobacter; however, this measure does not reduce levels to zero. • Cross-contamination awareness Prevention of cross-contamination by replacing cutlery and cutting boards used for food preparation after handling raw chicken and the prevention of hand contact with other foodstuffs after handling contaminated chicken meat considerably reduced Campylobacter contamination to other foods (Jong et al., 2008; Verhoeff-Bakkenes et al., 2008). Washing cutting boards and cutlery in hot water and detergent have greater effects on reducing Campylobacter contamination than using cold water (Jong et al., 2008). Reducing cross-contamination between materials contaminated with Campylobacter and other foods that may not receive further treatment (e.g. salad preparation) is especially important to preventing risks of infection (Verhoeff-Bakkenes et al., 2008). • Consumer education A large study showed that international recommendations to consumers is difficult. Particularly in terms of the lack of easy “rule-of-thumb” guidelines or tools to check CHAPTER 2 – CONTROL MEASURES 23 safe cooking conditions at home. The study concluded that regional differences in contamination levels, food culture and regional economies are challenges to developing international recommendations that ensure consumer food safety specific to Campylobacter infection risk that could be easily implemented by each country (Langsrud et al., 2020). Evaluation of web-based information interventions designed and tested on participant motivation and intentions to cook more safely was conducted (Nauta et al., 2008). The intervention supported by the emotion “disgust” was selected as the most promising information intervention. Alone, this intervention has no effect on infection risk but together with instructions for meal preparation, it was found that the risk decreased (Nauta et al., 2008). • Control measures in commercial kitchens Examination of Campylobacter contamination in restaurant kitchens reported that the prevalence of Campylobacter increased after raw meat handling. The prevalence of Campylobacter on food contact surfaces also increased, and in some cases the organism was present on food surfaces prior to raw meat preparation (Lai et al., 2021). Washing of boards and utensils in hot water and detergent was reported to reduce contamination, but poor washing hygiene practices did not reduce contamination (Lai et al., 2021; Jong et al., 2008). For commercial kitchens, poor sanitation offers greater opportunities for cross-contamination and Campylobacter transmission during preparation of chicken dishes (Lai et al., 2021). Use of neutral electrolyzed water (NEW), quaternary ammonium (QUAT), and lactic acid-based solutions on the surfaces of inoculated scarred polypropylene and wooden food-cutting boards reduced C. jejuni levels (Al-Qadiri et al., 2016). The reduction was dependent on contact time and the type of surface. These agents were found to cause reductions of 3 log on boards within the first minute of application and > 5 log reductions within 5 minutes of application. Reduction levels were lower on boards made of wood compared to polypropylene. In conclusion, the use of good hygiene practices and appropriate training of food handlers in food preparation kitchens that cater to mass events (restaurants) are essential to reduce the risk of cross-contamination between raw meats and finished (cooked products), and ultimately reduce the exposure of Campylobacter to consumers. In addition, the use of appropriate sanitizing agents and washing procedures for chopping boards, surfaces and kitchen tools is essential to reduce the risk of cross-contamination and human exposure. • Heating Studies using naturally contaminated chicken meat provide a more realistic model of treatments or interventions (e.g. cooking or processing) (Vaz et al. 2021). MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT24 Cooking at 70 °C was found to reduce Campylobacter levels by > 1.5 logs within 30 minutes (Vaz et al., 2021), but the organism survival persisted following initial reductions indicating that a core temperature is necessary to reduce Campylobacter to negligible levels. Heating to a core temperature > 74 °C has been shown to be required to reduce Campylobacter levels in cooked products (Sampers et al., 2010; FAO and WHO, 2011). • Marinades post-processing As with marination at broiler meat processing stage, marination of chicken products post-processing (e.g. consumer-based level) can reduce consumer risk of Campylobacter exposure. Some studies suggest Campylobacter reductions of 1–2 logs were possible using marinades, but such reductions are dependent on the concentration and type of ingredients used in the marinade (e.g. tartaric acid, oregano, thymol; essential oils). In one study, the effects of thyme oil extract in the marinade appeared to enhance the killing effect of Campylobacter resulting in a > 1 log reduction in inoculated chicken wings held at 4 °C for 168 h (Zakarienė et al., 2015). The spread of tartaric acid solutions (2, 4, 6 and 10 percent) on chicken meat was found to reduce the level of Campylobacter by 0.5 to 2 logs after storage for 3 days at 4 °C, but the studies were carried out in vitro and significant variation was observed among the 14 strains exposed to this acid (Birk et al., 2010). Apple-based edible films containing carvacrol and cinnamaldehyde were evaluated for bactericidal activity against antibiotic resistant and susceptible C. jejuni strains on chicken meat. Retail chicken breast samples inoculated with antibiotic resistant strains and a susceptible strain were wrapped in apple films containing cinnamaldehyde or carvacrol at 0.5 percent, 1.5 percent and 3 percent concentrations, and incubated at 4 or 23 °C for 72 h. The antimicrobial films exhibited dose- and temperature-dependent bactericidal activity against all tested strains. The films with cinnamaldehyde were more effective than carvacrol films, and reductions at 23 °C were greater than those at 4 °C. Populations of all strains were reduced to below detection level at 23 °C after 72 h exposure. At 4 °C cinnamaldehyde exposure reduced Campylobacter levels between 0.2 to 2.5 logs and 1.8 to 6.0 logs at concentrations of 1.5 percent and 3.0 percent, respectively (Mild et al., 2011). Interactions of Campylobacter with the microbial community throughout pre- and post-production processing are not yet well identified. A better understanding of the interactions between Campylobacter and the surrounding microbiota may further guide control measures support information used in qualitative and quantitative microbial risk assessments (QMRA) (Chintoan-Uta et al., 2022; Ijaz et al., 2018). 25 3 Review of the Code of Practice The expert committee was tasked with a review of the current code of practice with the view of assessing whether the current code of practice requires updates in light of new information or research or changes that require addressing or revision. The experts evaluated the impact or efficacy of control measures relevant to Campylobacter spp. in the broiler production chain, noting the variability of the impact reviewed and recommended revisions to the Guidelines for the Control of Campylobacter and Salmonella in Chicken Meat (CXG 78-2011), paragraphs 1 to 115, based on the currently available evidence (Annex 3).

27 4 Concluding remarks Since the first publications in the early 1970s showed an association between “Vibrios’’ (now named Campylobacters) in poultry and stool samples of humans with enteritis, tremendous efforts have been made to understand the infection from both the pathogen and the animal host side. Within broiler chicken production systems, various interventions throughout the process have been developed and evaluated. Although some successes have been reported, effective Campylobacter interventions are still very limited. Continuous research, innovation and collaboration among stakeholders are essential to further improve intervention strategies. The currently available interventions in broiler chicken pre- and post-production systems have been reviewed in this report as control measures for Campylobacter. As most of the burden of campylobacteriosis in humans is caused by C. jejuni and C. coli, the majority of available evidence is primarily reported on C. jejuni and C. coli species. For this report, the experts concentrated on the review and assessment of intervention measures to these two species. Several interventions have been proposed and tested, including the use of bacteriophages, vaccination, probiotics, and disinfectants, among others. Studies have also explored the effects of processing techniques, such as air chilling versus water chilling. Overall, the results of these studies have been mixed, with some interventions showing promise in reducing the prevalence of Campylobacter in specific stages of production, while others have had little to no effect. It is important to note MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT28 that interventions that have been successful in one study may not necessarily be effective in other settings, as the prevalence and characteristics of Campylobacter can vary widely between different processing facilities. The broader interventions at the primary production stage include precise biosecurity measures, such as strict hygiene practices and control of wildlife access to chicken farms. Targeted hazard-based interventions in the post-processing stages of production and good agriculture practices and hygienic practices for the general control of foodborne pathogens throughout the production system may be effective for the reduction of Campylobacter; however, there are no interventions that specifically control Campylobacter on meat. The experts recognize further data gaps exist and that some new technologies may offer promising approaches to reducing Campylobacter in pre- and post-production of chicken meat. Further global changes to the industry, growing of global populations, climate change, and increased demand for animal protein in specific regions will guide the need for further control measure assessments. In conclusion, while interventions to reduce Campylobacter in chicken processing have shown some promise, further research is needed to identify effective interventions that can be implemented on a large scale. It is also important to note that a multifaceted approach involving both pre- and post-harvest interventions is necessary to effectively control Campylobacter in chicken production systems, and an implementation of robust monitoring and surveillance systems to track Campylobacter throughout the system is crucial to evaluating the effectiveness of interventions and identifying emerging trends. 29 5 Intervention summary synopsis A number of interventions were identified through primary production to post-processing stages. The expert consultation concluded the following in each stage of production: Assessment of primary production interventions for the control of Campylobacter Biosecurity and management approaches • Using strict biosecurity measures (hygiene practices and sanitation) can enhance the control of Campylobacter in broiler flocks. • Risk factors for Campylobacter contamination at primary production establishments, such as partial depopulation, litter management, down period length, proximity to other livestock and slaughter age can help guide intervention strategies. Vaccination-based approaches • Currently, there are no commercial vaccines for Campylobacter readily available for any stage of primary production, and vaccination studies were limited to C. jejuni only. • Several potential vaccine candidates are in the proof-of-concept phase but cannot yet be considered as an intervention. • Some vaccines induced a cellular or humoral response in the chicken host, but this did not always translate to reduced caecal colonization by Campylobacter in pilot studies. 30 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Bacteriophage-based approaches • There are currently no commercial products available for use in primary production. • The effects of phage therapy may be transitory and prone to resistance. Feed and water additives Organic acids • In feed, short- and medium-chain fatty acids, and in particular, caprylic acid show promise as feed additives in reducing Campylobacter in pilot studies. • In water, organic acids reduced Campylobacter in caecal/faecal specimens at the end of the primary production period; however, the effects were not sustained to the end of production in pilot studies. Probiotics • In feed, there is inconsistent evidence on the efficacy of probiotics as an intervention for reducing Campylobacter in broilers at primary production level. Plant-based additives • In feed, the efficacy of some plant-based molecules in in vivo pilot studies showed limited reduction of Campylobacter in caecal/faecal specimens at the end of the primary production period. Assessment of processing interventions for the control of Campylobacter • Good hygiene practices during processing are important in minimizing Campylobacter contamination on meat. • The effectiveness of interventions during processing is dependent upon the incoming flock prevalence and concentration of Campylobacter in the gastrointestinal tract and on the bird. • The impact of processing practices can be enhanced by a combination of a multihurdle approach, processing effects, physical, and/or chemical interventions. Processing procedures • Logistic slaughter scheduling can reduce Campylobacter cross-contamination. • Scalding reduces the carcass surface concentration and prevalence of Campylobacter; however, the effect depends on the temperature, and dilution effect. CHAPTER 5 – INTERVENTION SUMMARY SYNOPSIS 31 • Defeathering and evisceration may increase both prevalence and concentration of Campylobacter on carcasses. • Immersion chilling can reduce the carcass concentration of Campylobacter; however, this is dependent on the initial Campylobacter load of incoming birds. • In combination with processing aids, immersion chilling may reduce the carcass prevalence of Campylobacter. • Air chilling may reduce concentration of Campylobacter, but the efficacy of air chilling in reducing the prevalence of Campylobacter when used without other processing aids is inconclusive. Physical • Irradiation is effective at eliminating Campylobacter on meat. • Freezing meat reduces the concentration of Campylobacter. • Steam, ultrasonication, high-intensity light pulse, visible light, UV-C and other technologies have shown promise either at the laboratory or pilot scale, but their impact is unknown at commercial scale. Chemical • Processing aids such as chlorine derivatives, peroxyacetic acids, and organic acids added to water used for washing and or dipping may reduce Campylobacter on carcasses. • Some marination ingredients have shown reductions in Campylobacter on meat. Assessment of post-processing interventions for the control of Campylobacter • Thorough cooking is effective at eliminating Campylobacter on meat. • The application of good hygiene practices is important in reducing Campylobacter on meat. • Freezing meat reduces the concentration of Campylobacter. • Some marination ingredients have shown reductions in Campylobacter on meat.

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Zoonoses and Public Health, 58(6): 440–447. https://doi.org/10.1111/j.1863-2378.2010.01387.x Umaraw, P., Prajapati, A., Verma, A.K., Pathak, V. & Singh, V.P. 2017. Control of campylobacter in poultry industry from farm to poultry processing unit: A review. Critical Reviews in Food Science and Nutrition, 57(4): 659–665. https://doi.org/10.1080/10408398.2014.935847 Urdaneta, S., Lorca-Oró, C., Dolz, R., López-Soria, S. & Cerdà-Cuéllar, M. 2023. In a warm climate, ventilation, indoor temperature and outdoor relative humidity have significant effects on Campylobacter spp. colonization in chicken broiler farms which can occur in only 2 days. Food Microbiology, 109: 104118. https://doi.org/10.1016/ j.fm.2022.104118 Van Gerwe, T., Bouma, A., Klinkenberg, D., Wagenaar, J.A., Jacobs- Reitsma, W.F. & Stegeman, A. 2010. Medium chain fatty acid feed supplementation reduces the probability of Campylobacter jejuni colonization in broilers. Veterinary Microbiology, 143(2–4): 314–318. https://doi.org/10.1016/j.vetmic.2009.11.029 van Wagenberg, C.P.A., Van Horne, P.L.M., Sommer, H.M. & Nauta, M.J. 2016. Cost-effectiveness of Campylobacter interventions on broiler farms in six European countries. Microbial Risk Analysis, 2–3: 53–62. https://doi. org/10.1016/j.mran.2016.05.003 CHAPTER 6 – REFERENCES 53 Vandeputte, J., Martel, A., Van Rysselberghe, N., Antonissen, G., Verlinden, M., De Zutter, L., Heyndrickx, M. et al. 2019. In ovo vaccination of broilers against Campylobacter jejuni using a bacterin and subunit vaccine. Poultry Science, 98(11): 5999–6004. https://doi.org/10.3382/ps/pez402 Vaz, C.S.L., Voss-Rech, D., Rebelatto, R., Duarte, S.C., Coldebella, A. & Bessa, M.C. 2021. Survival of Campylobacter jejuni in chicken at refrigeration and cooking temperatures. 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International Journal of Microbiology, 2022: 1–11. https://doi. org/10.1155/2022/1526641 54 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Williams, L.K., Sait, L.C., Trantham, E.K., Cogan, T.A. & Humphrey, T.J. 2013. Campylobacter infection has different outcomes in fast- and slow- growing broiler chickens. Avian Diseases, 57(2): 238–241. https://doi. org/10.1637/10442-110212-Reg.1 Wong, J.T., de Bruyn, J., Bagnol, B., Grieve, H., Li, M., Pym, R. & Alders, R.G. 2017. Small-scale poultry and food security in resource-poor settings: A review. Global Food Security, 15: 43–52. https://doi.org/10.1016/ j.gfs.2017.04.003 Zakarienė, G., Rokaitytė, A., Ramonaitė, S., Novoslavskij, A., Mulkytė, K., Zaborskienė, G. & Malakauskas, M. 2015. The antimicrobial effect of spice‐based marinades against Campylobacter jejuni on contaminated fresh broiler wings. Journal of Food Science, 80(3). https://doi. org/10.1111/1750-3841.12788 Zbrun, M.V., Rossler, E., Olivero, C.R., Soto, L.P., Zimmermann, J.A., Frizzo, L.S. & Signorini, M.L. 2021. Possible reservoirs of thermotolerant Campylobacter at the farm between rearing periods and after the use of enrofloxacin as a therapeutic treatment. International Journal of Food Microbiology, 340: 109046. https://doi.org/10.1016/ j.ijfoodmicro.2021.109046 Zweifel, C., Althaus, D. & Stephan, R. 2015. Effects of slaughter operations on the microbiological contamination of broiler carcasses in three abattoirs. Food Control, 51: 37–42. https://doi.org/10.1016/j.foodcont.2014.11.002 CHAPTER 1 – INTRODUCTION 55 Annex MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT CHAPTER 7 – ANNEX 57 THE KEYWORDS USED FOR SEARCHING THE CONTROL MEASURES OF CAMPYLOBACTER SPP. IN POULTRY Parameter Search 1 (poultry) poultry OR chicken* OR hen* OR broiler* OR “Gallus gallus” OR “Gallus domesticus” OR “G gallus” OR “G domesticus” OR “Gallus gallus domesticus” OR “G gallus domesticus” OR duck* OR turkey* OR goose OR geese OR guineafowl* OR pigeon* OR “quail” NOT layer* 2 (Salmonella) Campy or campylobacter 3 (intervention) intervention* OR antibiotic* OR antimicrobial* OR antibacterial* OR bacteriophage* OR bifidobac* OR biosecur* OR boning OR chlorine OR chill* OR “competitive exclusion” OR contamination Annex 1 58 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT 3 (intervention) OR control OR cool* OR cut* OR debon* OR decontaminat* OR decreas* OR dehid* OR dehair* OR disinfect* OR dress* OR efficacy OR eviserat* OR fabricat* OR grind* OR “hot water” OR hygiene OR immunis* OR immuniz* OR inactiv* OR irradiat* OR lactob* OR “lactic acid bacteria” OR mitigat* OR pasteuriz* OR phage* OR probiotic* OR reduce* OR reducing OR reduction OR rins* OR skin* OR “sodium chlorate” OR spray* OR steam OR treatment* OR storage OR trial OR trim* OR vaccin* OR vaccum* OR wash* 4 Title/Abstract (1 AND 2 AND 3) CHAPTER 7 – ANNEX 59 THE QUESTIONS FOR THE TWO-STEP RELEVANCE SCREENING AND CONFIRMATION A2.1 Relevance screening Question Options Key definitions 1. Does this citation describe research evaluating the efficacy and/or effectiveness (including costs or practically of implementation) of interventions to control Campylobacter in poultry at any stage from the primary production to consumption? Selections 1–3 will pass the citation to the next review stage and the article will be procured. • Yes, primary research • Yes, systematic review/ meta-analysis • Yes, risk assessment, risk profile, or other risk-based tool (e.g. cost-benefit analysis) • No, or it is a narrative literature review on the subject (exclude) Primary research is a collection of new data in a single study. Risk assessment is a scientifically based process consisting of the following steps: (i) hazard identification, (ii) hazard characterization, (iii) exposure assessment, and (iv) risk characterization. Risk profile presents the current state of knowledge related to a food safety issue, describes potential options that have been identified to date (if any), and the food safety policy context that will influence further possible actions. Other risk-based tools could include cost-benefit analyses, risk ranking, or risk prioritizations. Systematic review is a structured review of a clearly defined question with a transparent search strategy, relevance screening process, data extraction, risk-of-bias assessment and synthesis of results. Meta-analysis is a statistical technique that can be used on data collected in a systematic review. Exclude research on feral animals (e.g. feral pigs not produced for human consumption), and in vitro lab experiments. Annex 2 60 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT 2. What commodity is investigated? • Chicken (Gallus gallus domesticus) • Duck (Cairina sp) • Turkey (Meleagris) • Goose (Anser anser) • Guineafowl (Numida meleagris) • Pigeon (Columba livia domestica) • Quail (Coturnix japonica) • Other A2.2 Relevance confirmation Question Options Key definitions Did the study investigate outcomes other than Campylobacter? • Yes, E. coli (generic and/or pathogenic strains) • Yes, Salmonella • Yes, other bacteria • No In what setting was the study carried out? • Commercial/field conditions • Research farm/pilot plant • Smallholder farm/ abattoir conditions • Laboratory conditions • Not reported In what country was the study conducted? • The information is in the abstract, which is: (COMMENT) • Cannot tell from the abstract Specify country name only (not subregions, states, provinces, etc.) How much logarithm reduction? • The information is in the abstract, which is (COMMENT) • Cannot tell from the abstract • Other way to reflect the efficiency (COMMENT) CHAPTER 7 – ANNEX 61 Is it at farm? • Yes • No What is the intervention? • Biosecurity/ management practices • Vaccination • Antimicrobials • Competitive exclusion/ probiotics • Feed/water acidification • Feed characteristics/ management • Bacteriophages • Other (COMMENT) Antimicrobials: Examples include: Fluroquinolones, cephalosporins, gentamicin, ampicillin, tetracyclines, spectinomycin, ciprofloxacin, ceftriaxone. These may be administered via feed.  Biosecurity: This includes, but is not limited to, sanitation, biosafety, disinfection, hygiene and hygiene barriers, all- in-all-out production, depopulation, staff and the environment, litter testing and treatment, pest control, etc. Competitive exclusion: This may also be referred to as probiotics, prebiotics, and synbiotics. It may include Lactobacillus spp., bacteroides, Bifidobacterium spp., Enterococcus faecium, Aspergillus oryzae, and Saccharomyces spp. (S. cerevisiae, S. boulardii). It may be caecal contents or other materials from animals or the environment that contain many different or unknown bacterial species. Feed/water acidification: This is the addition of organic acids, such as lactic acid, to feed or water. It would include “nutraceuticals” such as copper, chromium, zinc, betaine or carnitine.  Feed management: These are, for example, comparisons of coarse/ finely ground feed, fermented feed, or liquid feed.  Segregated/logistic slaughter: For example, slaughtering/processing of more highly contaminated lots after less contaminated lots Standard processing procedures/good hygiene practices (GHP) refer to steps such as singeing, de- hiding, cooling, chilling, etc. Is it from transport to slaughter? • Yes • No What is the intervention? (COMMENT) Is it processing? • Yes • No What is the intervention? • Segregated/logistic slaughter • Cleaning/disinfection of equipment/ environments • Carcass/product washes, rinses, sprays • Standard processing procedures/good hygienic practices (GHP) • Irradiation • Modified packaging • Bacteriophages • Other (COMMENT) Is it from post- processing to consumer? • Yes • No What is the intervention? • Biosecurity/ management practices • Vaccination • Antimicrobials • Competitive exclusion/ probiotics • Feed/water acidification • Feed characteristics/ management • Bacteriophages • Other (COMMENT) 62 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT CHAPTER 7 – ANNEX 63 Recommended revisions to the Guidelines for the Control of Campylobacter and Salmonella in Chicken Meat (GXG 78-2011), as they relate specifically to the control of Campylobacter spp.  Para. CAC/GL 78-2011 JEMRA Recommendations 5. The Guidelines are presented in a flow diagram format so as to enhance practical application of a primary production-to-consumption approach to food safety. This format: • demonstrates differences and commonalities in approach for control measures for Campylobacter and Salmonella; • … ; and • facilitates development of HACCP plans at individual premises and national levels. • To consider updating the last bullet to read: “Facilitate development of HACCP and risk assessment plans at individual premises…” 9.  Scope  • Consider clarifying the scope to include: thermotolerant Campylobacter and non-Typhoidal Salmonella. 12. The Guidelines systematically present GHP-based control measures and examples of hazard- based control measures. GHP is a prerequisite to making choices on hazard-based control measures… Government and industry can use choices on hazard-based control measures to inform decisions on critical control points (CCPs) when applying HACCP principles to a particular food process. • Consider the following addition: “...(CCPs) and relative risk reduction when applying HACCP and risk assessment principles to a particular food process.” Annex 3 REVIEW OF THE CODEX GUIDELINES 64 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Para. CAC/GL 78-2011 JEMRA Recommendations 4. Definitions Support the following recommendation from the JEMRA meeting on Salmonella controls: • To consider including a definition for a production lot as per the Guidelines on the management of biological foodborne outbreaks. • Lot: A definite quantity of ingredients or of a food that is intended to have uniform character and quality, within specified limits, is produced, packaged and labelled under the same conditions, and is assigned a unique reference identification by the food business operator. It may also be referred to as a “batch”.  16. 5. PRINCIPLES APPLYING TO CONTROL OF CAMPYLOBACTER AND SALMONELLA IN CHICKEN MEAT Overarching.... i. The principles of food safety risk analysis should be incorporated wherever possible and appropriate in the control of Campylobacter and Salmonella in chicken meat from primary production to consumption. ii. Wherever possible and practical, Competent Authorities.... • Consider the following editorial change: “5i) The principles of food safety risk analysis should be incorporated to the extent possible and as appropriate...” and “5ii) To the extent possible and as appropriate, Competent Authorities should...” 18.  Food Safety Risk Profile for Salmonella species in broiler (young) chicken, June 2007.  Food Safety Risk Profile for Campylobacter species in broiler (young) chicken, June 2007.  Support the following recommendation from the JEMRA meeting on Salmonella controls: • To verify that the links referenced in the footnote are current and active.  • To evaluate paragraph 18 and to consider updating it, if needed.  CHAPTER 7 – ANNEX 65 Para. CAC/GL 78-2011 JEMRA Recommendations Section 7 PRIMARY PRODUCTION-TO- CONSUMPTION APPROACH TO CONTROL MEASURES Consider the following updates to account for religious practices that do not include stunning: • Process Flow Diagram 2: Step 14 - slaughter: B1) with stunning B2) without stunning, then A) Hang, then B1) split into Gas and Electrical Consider tick marks in Campylobacter column in the summary table for: • Receive at Slaughterhouse (use Establishment as a term) • Dress (interventions validated for Campylobacter during dressing (decontamination) • Portion (interventions directed at portions/parts) 24. Control of Campylobacter and Salmonella in grandparent flocks is strengthened by the application of a combination of biosecurity and personnel hygiene measures. The particular combination of control measures adopted at a national level should be determined in consultation with relevant stakeholders.  Support the following recommendation from the JEMRA meeting on Salmonella controls: • Consider including a definition for biosecurity that includes personal hygiene. • Consider aligning with the WOAH definition: https://www.woah.org/ fileadmin/Home/eng/Health_ standards/tahc/current/glossaire. pdf.  • Consider changing the text to read “…by the application of effective biosecurity measures.”  32. Personnel involved in the transportation of day-old chicks to parent flocks should not enter any livestock buildings and should prevent cross-contamination of day-old chicks during loading and unloading. • Consider updating the text to read: “…transportation of day-old chicks to parent flock establishments…’’ 36. Personnel involved in the transportation of day-old chicks should not enter any livestock buildings. • Consider changing “livestock buildings” to “…livestock establishments.” 66 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Para. CAC/GL 78-2011 JEMRA Recommendations 40. The use of fly screens to reduce or eliminate fly infestation in broiler houses has been shown to decrease the percentage of Campylobacter spp.-positive flocks from 51.4% to 15.4%. • Consider revising this guidance as there has not been any clear evidence since the initial studies on effectiveness. • Consider eliminating the percentages and leave the remainder of the statement. • Consider adding a statement to include fly screens, in combination with high biosecurity measures. 41. Full depopulation of the flock should be carried out where possible. Where this is not practicable and partial depopulation is practised, particular attention should be paid to strict biosecurity and hygiene of catchers and the equipment they use. • Consider adding the following to statement paragraph 41: “Partial depopulation has been shown to be a risk factor for the increase of Campylobacter contamination” as there are several reports on thinning/depopulation and Campylobacter contamination due to biosecurity deficiencies. 45. Where appropriate to the national situation, information about the flock, in particular about Salmonella and/or Campylobacter status should be provided in a timely manner to enable logistic slaughter and/ or channelling of poultry meat to treatment. • Consider replacing the word “treatment” with “reduced risk processing”, “intervention” or “custom processing”. 54.  Washing with abundant potable running water  Support the recommendations from the JEMRA meeting on Salmonella controls: • Consider replacing potable water with fit for purpose water to align with CXG1-1969, paragraph 70. Text should be adjusted to fit for purpose water. 59 Other factors that should be taken into account when designing process control systems that minimize contamination during scalding include: • degree of agitation; • use of multistaged tanks; • …; • tanks being cleaned and disinfected at least daily; and • hygiene measures applied to reused/recycled water. • Consider replacing “daily” with “tanks being cleaned and disinfected at an adequate frequency (e.g. end of shift)’’ • Consider adding the following bullet: “Directed water scalders” CHAPTER 7 – ANNEX 67 Para. CAC/GL 78-2011 JEMRA Recommendations 63. 9.4.1.5 Crop removal 63. Where possible, crops should be extracted in a manner that is likely to limit carcass contamination. • Consider adding the following to section 9.4.1.5: “The use of cropper systems allows the release of accumulated dirty water on the carcass cavity, so efforts to remove collected water prior to chilling should be considered.” 67. Carcass washing systems with 13 washers using water with 25-35 ppm total chlorine have been shown to reduce levels of Campylobacter by about 0.5 log10 CFU/ml of whole carcass rinse sample. Post-wash sprays using Acidified Sodium Chlorite (ASC) or TSP may further reduce Campylobacter levels by an average of 1.3 log10 CFU/ml or 1.0 log10 CFU/ml of whole carcass rinse samples respectively. Consider adding the following statement: “Carcass washes with 400 ppm paracetic acid (PAA), showed 1.2 log reductions of Campylobacter prior to chilling.” (Cano, Menses and Chaves, 2021; Chousalkar et al., 2019; De Villena et al., 2022; Dogan et al., 2019, 2022) 69. An on-line reprocessing spray system incorporating ASC has been shown to reduce Campylobacter in the whole carcass rinse sample by about 2.1 log10 CFU/ml and to reduce the prevalence of Salmonella positive carcasses from 37% to 10%. Consider adding the following statement: “Inside and outside bird washers used for online-reprocessing at 100 ppm of PAA showed 0.5 log reductions of Campylobacter.” (Cano, Menses and Chaves, 2021; Chousalkar et al., 2019; De Villena et al., 2022; Dogan et al., 2019) 70. Dipping carcasses in 10% TSP reduced Campylobacter by 1.7 log10 CFU/g neck skin and the MPN of Salmonella was reduced from 1.92 log10 CFU/g neck skin to undetectable levels. • Consider removing the recommendation for TSP since it may not be as commonly used at this time. • Consider adding the following statement: “Dip treatments in 200 ppm of PAA showed 1.4 log reductions of Campylobacter in carcass rinses.” (Cano, Menses and Chaves, 2021; Chousalkar et al., 2019; De Villena et al., 2022; Dogan et al., 2019) 68 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Para. CAC/GL 78-2011 JEMRA Recommendations 78. The use of chlorine in the chill tank may not act as a decontaminating agent by acting directly on the contaminated carcass. However, there would be a washing off effect by the water itself, and the addition of chlorine at a level sufficient to maintain a free residual in the water would then inactivate Campylobacter and Salmonella washed off, preventing re-attachment and cross- contamination. • Consider adding the following statement: “Immersion chillers using 225 ppm of PAA showed reductions of 1.18 log in concentration and a 76.5% reduction in prevalence of Campylobacter.” (Cano, Menses and Chaves, 2021; Chousalkar et al., 2019; De Villena et al., 2022; Dogan et al., 2022) 81. Forced air chilling (blast chilling) may reduce the concentration of Campylobacter on chicken carcasses by 0.4 log10 CFU/carcass. • Consider updating the value and excluding the unit of measure: “up to 1 log.” (ANSES, 2018) 82. Immersion chilling has been shown to reduce concentrations of Campylobacter by 1.1–1.3 log10 CFU/ ml of carcass rinse. • Consider updating this text to: “Immersion chilling reduces concentrations of Campylobacter, and with a combination of processing aids can result in a higher log reduction.” (Dogan et al., 2022) 84. Immersing whole carcasses in 600–800 ppm ASC at pH 2.5 to 2.7 for 15 seconds immediately post- chill, has been shown to reduce Campylobacter by 0.9–1.2 log10 CFU/ ml of whole carcass rinse sample. • Consider adding the following text: “Post chill tank interventions using sprays of PAA at 1 000 ppm showed up to 2.1 log reductions of Campylobacter.” (Cano, Menses and Chaves, 2021; Chousalkar et al., 2019; De Villena et al., 2022; Dogan et al., 2022) 9.10.1 For Campylobacter • Consider adding a new paragraph for Campylobacter and the following text: “Immersion of chicken wings in 1 000 ppm of PAA for 30 s has been shown to reduce 2.3 logs of Campylobacter” (Cano, Menses and Chaves, 2021; Chousalkar et al., 2019; De Villena et al., 2022; Dogan et al., 2022) CHAPTER 7 – ANNEX 69 Para. CAC/GL 78-2011 JEMRA Recommendations 94. Freezing of naturally contaminated carcasses followed by 31 days of storage at –20 degrees C has been shown to reduce Campylobacter by 0.7 to 2.9 log10 CFU/g. • Consider updating this statement to read: “Freezing of carcasses and portions contaminated with Campylobacter followed by storage at -20 degrees C has been shown to reduce Campylobacter by up to 2 logs” (Dogan et al., 2022). 95. Crust freezing using continuous carbon dioxide belt freezing of skinless breast fillets has been shown to give a reduction of Campylobacter of 0.4 log10 CFU/fillet. • Consider updating the statement to include all chicken meat products and not just skinless breast fillets. 108. Chicken meat should be cooked according to a process that is capable of achieving at least a 7 log reduction in both Campylobacter and Salmonella. • Consider updating the text to read: “Chicken meat should be cooked according to a process that is capable of reaching an internal temperature that can inactivate Salmonella and Campylobacter, for example 74 °C.” 115. Chicken meat should be cooked according to a process that is capable of achieving at least a 7 log reduction in both Campylobacter and Salmonella. • Consider updating the text to read: “Chicken meat should be cooked according to a process that is capable of reaching an internal temperature that can inactivate Salmonella and Campylobacter, for example 74 °C.” References: ANSES. 2018. State of knowledge relating to the contamination of broilers with Campylobacter and assessment of the impact of interventions at different stages of the food chain in France. Collective Expert Appraisal Report. 2016-SA-0183. Maisons-Alfort Cedex, France. https://www.anses.fr/en/ system/files/BIORISK2016SA0183RaEN.pdf Cano, C., Meneses, Y. & Chaves, B.D. 2021. Application of Peroxyacetic Acid for decontamination of raw poultry products and comparison to other commonly used chemical antimicrobial interventions: A review. Journal of Food Protection, 84(10): 1772–1783. https://doi.org/10.4315/JFP-21-107 70 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Chousalkar, K., Sims, S., McWhorter, A., Khan, S. & Sexton, M. 2019. The effect of sanitizers on microbial levels of chicken meat collected from commercial processing plants. International Journal of Environmental Research and Public Health, 16(23): 4807. https://doi.org/10.3390/ ijerph16234807 De Villena, J.F., Vargas, D.A., Bueno López, R., Chávez-Velado, D.R., Casas, D.E., Jiménez, R.L. & Sanchez-Plata, M.X. 2022. Bio-mapping indicators and pathogen loads in a commercial broiler processing facility operating with high and low antimicrobial intervention levels. Foods, 11(6): 775. https://doi.org/10.3390/foods11060775 Dogan, O.B., Aditya, A., Ortuzar, J., Clark, J. & Wang, B. 2022. A systematic review and meta-analysis of the efficacy of processing stages and interventions for controlling Campylobacter contamination during broiler chicken processing. Comprehensive Reviews in Food Science and Food Safety, 21(1): 227–271. https://doi.org/10.1111/1541-4337.12860 Dogan, O.B., Clarke, J., Mattos, F. & Wang, B. 2019. A quantitative microbial risk assessment model of Campylobacter in broiler chickens: Evaluating processing interventions. Food Control, 100: 97–110. https://doi. org/10.1016/j.foodcont.2019.01.003 CHAPTER 7 – ANNEX 71 BIBLIOGRAPHY USED FOR SCOPING REVIEW A 4.1 Primary A4.1.1 Biosecurity and management approaches Agunos, A., Waddell, L., Léger, D. & Taboada, E. 2014. 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Molecular Ecology, 22(5): 1463– 1472. https://doi.org/10.1111/mec.12144 Guerin, M.T., Martin, S.W., Reiersen, J., Berke, O., McEwen, S.A., Friðriksdóttir, V., Bisaillon, J.-R. & Lowman, R. 2008. Temperature- related risk factors associated with the colonization of broiler-chicken flocks with Campylobacter spp. in Iceland, 2001–2004. Preventive Veterinary Medicine, 86(1–2): 14–29. https://doi.org/10.1016/ j.prevetmed.2008.02.015 Hansson, I., Olsson Engvall, E., Vågsholm, I. & Nyman, A. 2010. Risk factors associated with the presence of Campylobacter-positive broiler flocks in Sweden. Preventive Veterinary Medicine, 96:114-121. doi: 10.1016/ j.prevetmed.2010.05.007 Hasan, Md.M., Talukder, S., Mandal, A.K., Tasmim, S.T., Parvin, Mst.S., Ali, Md.Y., Sikder, M.H. & Islam, Md.T. 2020. Prevalence and risk factors of Campylobacter infection in broiler and cockerel flocks in Mymensingh and Gazipur districts of Bangladesh. 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Impact of industrial production system parameters on chicken microbiomes: mechanisms to improve performance and reduce Campylobacter. Microbiome, 8(1): 128. https://doi.org/10.1186/s40168- 020-00908-8 Mendes, Â.J., Santos-Ferreira, N.L., Costa, F.M., Lopes, E.P., Freitas-Silva, J., Inácio, Â.S., Moreira, F. & Martins Da Costa, P. 2020. External contamination of broilers by Campylobacter spp. increases from the farm to the slaughterhouse. British Poultry Science, 61(4): 400–407. https://doi. org/10.1080/00071668.2020.1736264 CHAPTER 7 – ANNEX 75 Näther, G., Alter, T., Martin, A. & Ellerbroek, L. 2009. Analysis of risk factors for Campylobacter species infection in broiler flocks. Poultry Science, 88(6): 1299–1305. https://doi.org/10.3382/ps.2008-00389 Natsos, G., Mouttotou, N.K., Magiorkinis, E., Ioannidis, A., Rodi-Burriel, A., Chatzipanagiotou, S. & Koutoulis, K.C. 2020. Prevalence of and risk factors for Campylobacter spp. colonization of broiler chicken flocks in Greece. 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Poultry Science, 96(1): 184–191. https://doi.org/10.3382/ps/ pew277 Schweitzer, P.M., Susta, L., Varga, C., Brash, M.L. & Guerin, M.T. 2021. Demographic, husbandry, and biosecurity factors associated with the presence of Campylobacter spp. in small poultry flocks in Ontario, Canada. Pathogens, 10(11): 1471. https://doi.org/10.3390/ pathogens10111471 Sevilla‐Navarro, S., Marin, C., Cortés, V., García, C. & Catalá‐Gregori, P. 2020. Campylobacter prevalence and risk factors associated with exceeding allowable limits in poultry slaughterhouses in Spain. Veterinary Record, 186(13): 415–415. https://doi.org/10.1136/vr.105558 Sheppard, S.K., Colles, F., Richardson, J., Cody, A.J., Elson, R., Lawson, A., Brick, G. et al. 2010. Host association of Campylobacter genotypes transcends geographic variation. Applied and Environmental Microbiology, 76(15): 5269–5277. https://doi.org/10.1128/AEM.00124-10 76 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Smith, S., Messam, L.L.McV., Meade, J., Gibbons, J., McGill, K., Bolton, D. & Whyte, P. 2016. The impact of biosecurity and partial depopulation on Campylobacter prevalence in Irish broiler flocks with differing levels of hygiene and economic performance. Infection Ecology & Epidemiology, 6(1): 31454. https://doi.org/10.3402/iee.v6.31454 Torralbo, A., Borge, C., Allepuz, A., García-Bocanegra, I., Sheppard, S.K., Perea, A. & Carbonero, A. 2014. Prevalence and risk factors of Campylobacter infection in broiler flocks from southern Spain. Preventive Veterinary Medicine, 114(2): 106–113. https://doi.org/10.1016/ j.prevetmed.2014.01.019 Urdaneta, S., Lorca-Oró, C., Dolz, R., López-Soria, S. & Cerdà-Cuéllar, M. 2023. In a warm climate, ventilation, indoor temperature and outdoor relative humidity have significant effects on Campylobacter spp. colonization in chicken broiler farms which can occur in only 2 days. Food Microbiology, 109: 104118. https://doi.org/10.1016/ j.fm.2022.104118 van Wagenberg, C.P.A., Van Horne, P.L.M., Sommer, H.M. & Nauta, M.J. 2016. Cost-effectiveness of Campylobacter interventions on broiler farms in six European countries. Microbial Risk Analysis, 2–3: 53–62. https://doi. org/10.1016/j.mran.2016.05.003 Wanja, D.W., Mbuthia, P.G., Aboge, G.O. & Bebora, L.C. 2022. Seasonal prevalence and molecular identification of thermophilic Campylobacter from chicken, cattle, and respective drinking water in Kajiado County, Kenya. International Journal of Microbiology, 2022: 1–11. https://doi. org/10.1155/2022/1526641 Williams, L.K., Sait, L.C., Trantham, E.K., Cogan, T.A. & Humphrey, T.J. 2013. Campylobacter infection has different outcomes in fast- and slow- growing broiler chickens. Avian Diseases, 57(2): 238–241. https://doi. org/10.1637/10442-110212-Reg.1 Zbrun, M.V., Rossler, E., Olivero, C.R., Soto, L.P., Zimmermann, J.A., Frizzo, L.S. & Signorini, M.L. 2021. Possible reservoirs of thermotolerant Campylobacter at the farm between rearing periods and after the use of enrofloxacin as a therapeutic treatment. International Journal of Food Microbiology, 340: 109046. https://doi.org/10.1016/ j.ijfoodmicro.2021.109046 CHAPTER 7 – ANNEX 77 A4.1.2 Vaccine and phage-based approaches Vaccine Buckley, A.M., Wang, J., Hudson, D.L., Grant, A.J., Jones, M.A., Maskell, D.J. & Stevens, M.P. 2010. Evaluation of live-attenuated Salmonella vaccines expressing Campylobacter antigens for control of C. jejuni in poultry. Vaccine, 28(4): 1094–1105. https://doi.org/10.1016/j.vaccine.2009.10.018 Chintoan-Uta, C., Cassady-Cain, R.L. & Stevens, M.P. 2016. Evaluation of flagellum-related proteins FliD and FspA as subunit vaccines against Campylobacter jejuni colonisation in chickens. Vaccine, 34(15): 1739– 1743. https://doi.org/10.1016/j.vaccine.2016.02.052 Clark, J.D., Oakes, R.D., Redhead, K., Crouch, C.F., Francis, M.J., Tomley, F.M. & Blake, D.P. 2012. Eimeria species parasites as novel vaccine delivery vectors: Anti-Campylobacter jejuni protective immunity induced by Eimeria tenella-delivered CjaA. Vaccine, 30(16): 2683–2688. https://doi. org/10.1016/j.vaccine.2012.02.002 Cui, Y., Guo, F., Guo, J., Cao, X., Wang, H., Yang, B., Zhou, H. et al. 2020. Immunization of chickens with the Enterobactin conjugate vaccine reduced Campylobacter jejuni colonization in the intestine. Vaccines, 8(4): 747. https://doi.org/10.3390/vaccines8040747 Gloanec, N., Dory, D., Quesne, S., Béven, V., Poezevara, T., Keita, A., Chemaly, M. & Guyard-Nicodème, M. 2022. Impact of DNA prime/protein boost vaccination against Campylobacter jejuni on immune responses and gut microbiota in chickens. Vaccines, 10(6): 981. https://doi.org/10.3390/ vaccines10060981 Jeon, B., Saisom, T., Sasipreeyajan, J. & Luangtongkum, T. 2022. Live- attenuated oral vaccines to reduce Campylobacter colonization in poultry. Vaccines, 10(5): 685. https://doi.org/10.3390/vaccines10050685 Łaniewski, P., Kuczkowski, M., Chrząstek, K., Woźniak, A., Wyszyńska, A., Wieliczko, A. & Jagusztyn-Krynicka, E.K. 2014. Evaluation of the immunogenicity of Campylobacter jejuni CjaA protein delivered by Salmonella enterica sv. Typhimurium strain with regulated delayed attenuation in chickens. World Journal of Microbiology and Biotechnology, 30(1): 281–292. https://doi.org/10.1007/s11274-013-1447-5 78 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Layton, S.L., Morgan, M.J., Cole, K., Kwon, Y.M., Donoghue, D.J., Hargis, B.M. & Pumford, N.R. 2011. Evaluation of Salmonella-vectored Campylobacter peptide epitopes for reduction of Campylobacter jejuni in broiler chickens. Clinical and Vaccine Immunology, 18(3): 449–454. https://doi.org/10.1128/CVI.00379-10 Mauri, M., Sannasiddappa, T.H., Vohra, P., Corona-Torres, R., Smith, A.A., Chintoan-Uta, C., Bremner, A. et al. 2021. Multivalent poultry vaccine development using Protein Glycan Coupling Technology. Microbial Cell Factories, 20(1): 193. https://doi.org/10.1186/s12934-021-01682-4 Meunier, M., Guyard-Nicodème, M., Vigouroux, E., Poezevara, T., Béven, V., Quesne, S., Amelot, M. et al. 2018. A DNA prime/protein boost vaccine protocol developed against Campylobacter jejuni for poultry. Vaccine, 36(16): 2119–2125. https://doi.org/10.1016/j.vaccine.2018.03.004 Nothaft, H., Perez-Muñoz, M.E., Yang, T., Murugan, A.V.M., Miller, M., Kolarich, D., Plastow, G.S., Walter, J. & Szymanski, C.M. 2021. Improving chicken responses to glycoconjugate vaccination against Campylobacter jejuni. Frontiers in Microbiology, 12: 734526. https://doi. org/10.3389/fmicb.2021.734526 Radomska, K.A., Vaezirad, M.M., Verstappen, K.M., Wösten, M.M.S.M., Wagenaar, J.A. & Van Putten, J.P.M. 2016. Chicken immune response after In Ovo immunization with Chimeric TLR5 activating flagellin of Campylobacter jejuni. PLoS ONE, 11(10): e0164837. https://doi. org/10.1371/journal.pone.0164837 Thibodeau, A., Fravalo, P., Perron, A., Lewandowski, S.L.- & Letellier, A. 2017. Production and characterization of anti-Campylobacter jejuni IgY derived from egg yolks. Acta Veterinaria Scandinavica, 59(1): 80. https:// doi.org/10.1186/s13028-017-0346-4 Vandeputte, J., Martel, A., Van Rysselberghe, N., Antonissen, G., Verlinden, M., De Zutter, L., Heyndrickx, M. et al. 2019. In ovo vaccination of broilers against Campylobacter jejuni using a bacterin and subunit vaccine. Poultry Science, 98(11): 5999–6004. https://doi.org/10.3382/ps/pez402 Phage Carvalho, C.M., Gannon, B.W., Halfhide, D.E., Santos, S.B., Hayes, C.M., Roe, J.M. & Azeredo, J. 2010. The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiology, 10(1): 232. https:// doi.org/10.1186/1471-2180-10-232 CHAPTER 7 – ANNEX 79 Chinivasagam, H.N., Estella, W., Maddock, L., Mayer, D.G., Weyand, C., Connerton, P.L. & Connerton, I.F. 2020. Bacteriophages to control Campylobacter in commercially farmed broiler chickens, in Australia. Frontiers in Microbiology, 11: 632. https://doi.org/10.3389/ fmicb.2020.00632 D’Angelantonio, D., Scattolini, S., Boni, A., Neri, D., Di Serafino, G., Connerton, P., Connerton, I. et al. 2021. Bacteriophage therapy to reduce colonization of Campylobacter jejuni in broiler chickens before slaughter. Viruses, 13(8): 1428. https://doi.org/10.3390/v13081428 El-Shibiny, A., Scott, A., Timms, A., Metawea, Y., Connerton, P. & Connerton, I. 2009. Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. Journal of Food Protection, 72(4): 733–740. https://doi. org/10.4315/0362-028X-72.4.733 Fischer, S., Kittler, S., Klein, G. & Glünder, G. 2013. Impact of a single phage and a phage cocktail application in broilers on reduction of Campylobacter jejuni and development of resistance. PLoS ONE, 8(10): e78543. https://doi.org/10.1371/journal.pone.0078543 Furuta, M., Nasu, T., Umeki, K., Hoang Minh, D., Honjoh, K.-I. & Miyamoto, T. 2017. Characterization and application of Lytic bacteriophages against Campylobacter jejuni isolated from poultry in Japan. Biocontrol Science, 22(4): 213–221. https://doi.org/10.4265/bio.22.213 Hammerl, J.A., Jäckel, C., Alter, T., Janzcyk, P., Stingl, K., Knüver, M.T. & Hertwig, S. 2014. Reduction of Campylobacter jejuni in broiler chicken by successive application of group II and group III phages. PLoS ONE, 9(12): e114785. https://doi.org/10.1371/journal.pone.0114785 Kittler, S., Fischer, S., Abdulmawjood, A., Glünder, G. & Klein, G. 2013. Effect of bacteriophage application on Campylobacter jejuni loads in commercial broiler flocks. Applied and Environmental Microbiology, 79(23): 7525–7533. https://doi.org/10.1128/AEM.02703-13 Richards, P.J., Connerton, P.L. & Connerton, I.F. 2019. Phage biocontrol of Campylobacter jejuni in chickens does not produce collateral effects on the gut microbiota. Frontiers in Microbiology, 10: 476. https://doi. org/10.3389/fmicb.2019.00476 80 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT A4.1.3 Feed and water additives approaches Caprylic acid and other organic acids Currie, D., Green, M., Dufailu, O.A., Matthaios, P., Soultanas, P., McCartney, E., Lester, H. et al. 2018. Dietary supplementation with ferric tyrosine improves zootechnical performance and reduces caecal Campylobacter spp. load in broilers. British Poultry Science, 59(6): 646–653. https://doi. org/10.1080/00071668.2018.1507015 De Los Santos, F.S., Donoghue, A.M., Venkitanarayanan, K., Dirain, M.L., Reyes-Herrera, I., Blore, P.J. & Donoghue, D.J. 2008. Caprylic acid supplemented in feed reduces Enteric Campylobacter jejuni colonization in ten-day-old broiler chickens. Poultry Science, 87(4): 800–804. https:// doi.org/10.3382/ps.2007-00280 De Los Santos, F.S., Donoghue, A.M., Venkitanarayanan, K., Metcalf, J.H., Reyes-Herrera, I., Dirain, M.L., Aguiar, V.F., Blore, P.J. & Donoghue, D.J. 2009. The natural feed additive caprylic acid decreases Campylobacter jejuni colonization in market-aged broiler chickens. Poultry Science, 88(1): 61–64. https://doi.org/10.3382/ps.2008-00228 De Los Santos, F.S., Donoghue, A.M., Venkitanarayanan, K., Reyes-Herrera, I., Metcalf, J.H., Dirain, M.L., Aguiar, V.F., Blore, P.J. & Donoghue, D.J. 2008. Therapeutic supplementation of caprylic acid in feed reduces Campylobacter jejuni colonization in broiler chicks. Applied and Environmental Microbiology, 74(14): 4564–4566. https://doi.org/10.1128/ AEM.02528-07 De Los Santos, F.S., Hume, M., Venkitanarayanan, K., Donoghue, A.M., Hanning, I., Slavik, M.F., Aguiar, V.F. et al. 2010. Caprylic acid reduces enteric Campylobacter colonization in market-aged broiler chickens but does not appear to alter cecal microbial populations. Journal of Food Protection, 73(2): 251–257. https://doi.org/10.4315/0362-028X-73.2.251 Greene, G., Koolman, L., Whyte, P., Lynch, H., Coffey, A., Lucey, B., Egan, J., O’Connor, L. & Bolton, D. 2022. The efficacy of organic acid, medium chain fatty acid and essential oil based broiler treatments; in vitro anti‐ Campylobacter jejuni activity and the effect of these chemical‐based treatments on broiler performance. Journal of Applied Microbiology, 132(1): 687–695. https://doi.org/10.1111/jam.15204 CHAPTER 7 – ANNEX 81 Hovorková, P. & Skřivanová, E. 2015. Use of Caprylic acid in broiler chickens: effect on Campylobacter jejuni. Foodborne Pathogens and Disease, 12(8): 712–718. https://doi.org/10.1089/fpd.2015.1978 Khattak, F., Paschalis, V., Green, M., Houdijk, J.G.M., Soultanas, P. & Mahdavi, J. 2018. TYPLEX® Chelate, a novel feed additive, inhibits Campylobacter jejuni biofilm formation and cecal colonization in broiler chickens. Poultry Science, 97(4): 1391–1399. https://doi.org/10.3382/ps/pex413 Metcalf, J.H., Donoghue, A.M., Venkitanarayanan, K., Reyes-Herrera, I., Aguiar, V.F., Blore, P.J. & Donoghue, D.J. 2011. Water administration of the medium-chain fatty acid caprylic acid produced variable efficacy against enteric Campylobacter colonization in broilers 1, 2. Poultry Science, 90(2): 494–497. https://doi.org/10.3382/ps.2010-00891 Probiotics Arsi, K., Donoghue, A.M., Woo-Ming, A., Blore, P.J. & Donoghue, D.J. 2015. The efficacy of selected probiotic and prebiotic combinations in reducing Campylobacter colonization in broiler chickens. Journal of Applied Poultry Research, 24(3): 327–334. https://doi.org/10.3382/japr/pfv032 Cean, A., Stef, L., Simiz, E., Julean, C., Dumitrescu, G., Vasile, A., Pet, E., Drinceanu, D. & Corcionivoschi, N. 2015. Effect of human isolated probiotic bacteria on preventing Campylobacter jejuni colonization of poultry. Foodborne Pathogens and Disease, 12(2): 122–130. https://doi. org/10.1089/fpd.2014.1849 Dec, M., Nowaczek, A., Urban-Chmiel, R., Stępień-Pyśniak, D. & Wernicki, A. 2018. Probiotic potential of Lactobacillus isolates of chicken origin with anti-Campylobacter activity. Journal of Veterinary Medical Science, 80(8): 1195–1203. https://doi.org/10.1292/jvms.18-0092 Froebel, L.K., Jalukar, S., Lavergne, T.A., Coufal, C.D. & Duong, T. 2020. Administration of direct-fed Bacillus cultures and refined functional carbohydrates to broiler chickens improves growth performance and promotes positive shifts in gastrointestinal microbiota. Journal of Applied Poultry Research, 29(4): 765–774. https://doi.org/10.1016/ j.japr.2020.06.004 82 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Ghareeb, K., Awad, W.A., Mohnl, M., Porta, R., Biarnés, M., Böhm, J. & Schatzmayr, G. 2012. Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens. Poultry Science, 91(8): 1825–1832. https://doi.org/10.3382/ ps.2012-02168 Gharib Naseri, K., Rahimi, S. & Khaki, P. 2012. Comparison of the effects of probiotic, organic acid and medicinal plant on Campylobacter jejuni challenged broiler chickens. Journal of Agricultural Science and Technology, 14(7): 1485–1496. Gorain, C., Singh, A., Bhattacharyya, S., Kundu, A., Lahiri, A., Gupta, S. & Mallick, A.I. 2020. Mucosal delivery of live Lactococcus lactis expressing functionally active JlpA antigen induces potent local immune response and prevent enteric colonization of Campylobacter jejuni in chickens. Vaccine, 38(7): 1630–1642. https://doi.org/10.1016/j.vaccine.2019.12.064 Guo, J.R., Dong, X.F., Liu, S. & Tong, J.M. 2018. High-throughput sequencing reveals the effect of Bacillus subtilis CGMCC 1.921 on the cecal microbiota and gene expression in ileum mucosa of laying hens. Poultry Science, 97(7): 2543–2556. https://doi.org/10.3382/ps/pey112 Khan, M. 2019. Effect of newly characterized probiotic lactobacilli on weight gain, immunomodulation and gut microbiota of Campylobacter jejuni challenged broiler chicken. Pakistan Veterinary Journal, 39(04): 473–478. https://doi.org/10.29261/pakvetj/2019.051 Massacci, F.R., Lovito, C., Tofani, S., Tentellini, M., Genovese, D.A., De Leo, A.A.P., Papa, P. et al. 2019. Dietary saccharomyces cerevisiae boulardii CNCM I-1079 positively affects performance and intestinal ecosystem in broilers during a Campylobacter jejuni infection. Microorganisms, 7(12): 596. https://doi.org/10.3390/microorganisms7120596 Mortada, M., Cosby, D.E., Shanmugasundaram, R. & Selvaraj, R.K. 2020. In vivo and in vitro assessment of commercial probiotic and organic acid feed additives in broilers challenged with Campylobacter coli. Journal of Applied Poultry Research, 29(2): 435–446. https://doi.org/10.1016/ j.japr.2020.02.001 Nazef, L., Belguesmia, Y., Tani, A., Prévost, H. & Drider, D. 2008. Identification of lactic acid bacteria from poultry feces: evidence on anti-Campylobacter and anti-Listeria activities. Poultry Science, 87(2): 329–334. https://doi. org/10.3382/ps.2007-00282 CHAPTER 7 – ANNEX 83 Saint-Cyr, M.J., Haddad, N., Taminiau, B., Poezevara, T., Quesne, S., Amelot, M., Daube, G. et al. 2017. Use of the potential probiotic strain Lactobacillus salivarius SMXD51 to control Campylobacter jejuni in broilers. International Journal of Food Microbiology, 247: 9–17. https:// doi.org/10.1016/j.ijfoodmicro.2016.07.003 Śmiałek, M., Kowalczyk, J. & Koncicki, A. 2021. The use of probiotics in the reduction of Campylobacter spp. prevalence in poultry. Animals, 11(5): 1355. https://doi.org/10.3390/ani11051355 Szott, V., Reichelt, B., Friese, A. & Roesler, U. 2022. A complex competitive exclusion culture reduces Campylobacter jejuni colonization in broiler chickens at slaughter age in vivo. Veterinary Sciences, 9(4): 181. https:// doi.org/10.3390/vetsci9040181 Tabashsum, Z., Peng, M., Alvarado-Martinez, Z., Aditya, A., Bhatti, J., Romo, P.B., Young, A. & Biswas, D. 2020. Competitive reduction of poultry-borne enteric bacterial pathogens in chicken gut with bioactive Lactobacillus casei. Scientific Reports, 10(1): 16259. https://doi. org/10.1038/s41598-020-73316-5 Ty, M., Taha-Abdelaziz, K., Demey, V., Castex, M., Sharif, S. & Parkinson, J. 2022. Performance of distinct microbial based solutions in a Campylobacter infection challenge model in poultry. Animal Microbiome, 4(1): 2. https://doi.org/10.1186/s42523-021-00157-6 Willis, W.L. & Reid, L. 2008. Investigating the effects of dietary probiotic feeding regimens on broiler chicken production and Campylobacter jejuni presence. Poultry Science, 87(4): 606–611. https://doi.org/10.3382/ ps.2006-00458 Yuri Kuznetsov, I.N. 2020. Evaluation lactic acid bacteria autostrains with anti-Campylobacter jejuni activity on broiler chickens productivity. International Transaction Journal of Engineering, Management: 11A15S: 15. https://doi.org/10.14456/ITJEMAST.2020.307 The addition of plant-based molecules to feed Allaoua, M., Bonnafé, E., Etienne, P., Noirot, V., Gabarrou, J.-F., Castinel, A., Pascal, G. et al. 2022. A carvacrol-based product reduces Campylobacter jejuni load and alters microbiota composition in the caeca of chickens. Journal of Applied Microbiology, 132(6): 4501–4516. https://doi. org/10.1111/jam.15521 84 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Allaoua, M., Etienne, P., Noirot, V., Carayon, J.-L., Téné, N., Bonnafé, E. & Treilhou, M. 2018. Pharmacokinetic and antimicrobial activity of a new carvacrol-based product against a human pathogen, Campylobacter jejuni. Journal of Applied Microbiology, 125(4): 1162–1174. https://doi. org/10.1111/jam.13915 Arsi, K., Donoghue, A.M., Venkitanarayanan, K., Kollanoor‐Johny, A., Fanatico, A.C., Blore, P.J. & Donoghue, D.J. 2014. The efficacy of the natural plant extracts, thymol and carvacrol against Campylobacter colonization in broiler chickens. Journal of Food Safety, 34(4): 321–325. https://doi.org/10.1111/jfs.12129 Arsi, K., Donoghue, A.M., Woo-Ming, A., Blore, P.J. & Donoghue, D.J. 2015. The efficacy of selected probiotic and prebiotic combinations in reducing Campylobacter colonization in broiler chickens. Journal of Applied Poultry Research, 24(3): 327–334. https://doi.org/10.3382/japr/pfv032 Epps, S.V.R., Harvey, R.B., Byrd, J.A., Petrujkić, B.T., Sedej, I., Beier, R.C., Phillips, T.D. et al. 2015. Comparative effect of thymol or its glucose conjugate, thymol-β- d -glucopyranoside, on Campylobacter in avian gut contents. Journal of Environmental Science and Health, Part B, 50(1): 55–61. https://doi.org/10.1080/03601234.2015.965634 Friedman, M. 2017. Chemistry, antimicrobial mechanisms, and antibiotic activities of cinnamaldehyde against pathogenic bacteria in animal feeds and human foods. Journal of Agricultural and Food Chemistry, 65(48): 10406–10423. https://doi.org/10.1021/acs.jafc.7b04344 Gharib Naseri, K., Rahimi, S. & Khaki, P. 2012. Comparison of the effects of probiotic, organic acid and medicinal plant on Campylobacter jejuni challenged broiler chickens. Journal of Agricultural Science and Technology, 14(7): 1485–1496. Hankel, J., Popp, J., Meemken, D., Zeiger, K., Beyerbach, M., Taube, V., Klein, G. & Visscher, C. 2018. Influence of lauric acid on the susceptibility of chickens to an experimental Campylobacter jejuni colonisation. PLoS ONE, 13(9): e0204483. https://doi.org/10.1371/journal.pone.0204483 Ibrahim, D., Sewid, A.H., Arisha, A.H., Abd El-fattah, A.H., Abdelaziz, A.M., Al-Jabr, O.A. & Kishawy, A.T.Y. 2020. Influence of Glycyrrhiza glabra extract on growth, gene expression of gut integrity, and Campylobacter jejuni colonization in broiler chickens. Frontiers in Veterinary Science, 7: 612063. https://doi.org/10.3389/fvets.2020.612063 CHAPTER 7 – ANNEX 85 Kollanoor Johny, A., Darre, M.J., Donoghue, A.M., Donoghue, D.J. & Venkitanarayanan, K. 2010. Antibacterial effect of trans- cinnamaldehyde, eugenol, carvacrol, and thymol on Salmonella Enteritidis and Campylobacter jejuni in chicken cecal contents in vitro. Journal of Applied Poultry Research, 19(3): 237–244. https://doi. org/10.3382/japr.2010-00181 Kurekci, C., Al Jassim, R., Hassan, E., Bishop-Hurley, S.L., Padmanabha, J. & McSweeney, C.S. 2014. Effects of feeding plant-derived agents on the colonization of Campylobacter jejuni in broiler chickens. Poultry Science, 93(9): 2337–2346. https://doi.org/10.3382/ps.2014-03950 Lee, N.-K., Jung, B.S., Na, D.S., Yu, H.H., Kim, J.-S. & Paik, H.-D. 2016. The impact of antimicrobial effect of chestnut inner shell extracts against Campylobacter jejuni in chicken meat. LWT - Food Science and Technology, 65: 746–750. https://doi.org/10.1016/j.lwt.2015.09.004 Salaheen, S., Tabashsum, Z., Gaspard, S., Dattilio, A., Tran, T.H. & Biswas, D. 2018. Reduced Campylobacter jejuni colonization in poultry gut with bioactive phenolics. Food Control, 84: 1–7. https://doi.org/10.1016/ j.foodcont.2017.07.021 Szott, V., Reichelt, B., Alter, T., Friese, A. & Roesler, U. 2020. In vivo efficacy of carvacrol on Campylobacter jejuni prevalence in broiler chickens during an entire fattening period. European Journal of Microbiology and Immunology, 10(3): 131–138. https://doi.org/10.1556/1886.2020.00011 Tolnai, E., Fauszt, P., Fidler, G., Pesti-Asboth, G., Szilagyi, E., Stagel, A., Konya, J. et al. 2021. Nutraceuticals induced changes in the broiler gastrointestinal tract microbiota. mSystems, 6(2): e01124-20. https://doi. org/10.1128/mSystems.01124-20 Wagle, B.R., Donoghue, A.M., Shrestha, S., Upadhyaya, I., Arsi, K., Gupta, A., Liyanage, R. et al. 2020. Carvacrol attenuates Campylobacter jejuni colonization factors and proteome critical for persistence in the chicken gut. Poultry Science, 99(9): 4566–4577. https://doi.org/10.1016/ j.psj.2020.06.020 Zeiger, K., Popp, J., Becker, A., Hankel, J., Visscher, C., Klein, G. & Meemken, D. 2017. Lauric acid as feed additive – An approach to reducing Campylobacter spp. in broiler meat. PLoS ONE, 12(4): e0175693. https:// doi.org/10.1371/journal.pone.0175693 86 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT In water plant-based additives and organic acids Ghareeb, K., Awad, W.A., Mohnl, M., Porta, R., Biarnés, M., Böhm, J. & Schatzmayr, G. 2012. Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens. Poultry Science, 91(8): 1825–1832. https://doi.org/10.3382/ ps.2012-02168 Gharib Naseri, K., Rahimi, S. & Khaki, P. 2012. Comparison of the effects of probiotic, organic acid and medicinal plant on Campylobacter jejuni challenged broiler chickens. Journal of Agricultural Science and Technology, 14(7): 1485–1496. Johny, A.K., Darre, M.J., Hoagland, T.A., Schreiber, D.T., Donoghue, A.M., Donoghue, D.J. & Venkitanarayanan, K. 2008. Antibacterial effect of trans-cinnamaldehyde on Salmonella Enteritidis and Campylobacter jejuni in chicken drinking water. Journal of Applied Poultry Research, 17(4): 490–497. https://doi.org/10.3382/japr.2008-00051 Metcalf, J.H., Donoghue, A.M., Venkitanarayanan, K., Reyes-Herrera, I., Aguiar, V.F., Blore, P.J. & Donoghue, D.J. 2011. Water administration of the medium-chain fatty acid caprylic acid produced variable efficacy against enteric Campylobacter colonization in broilers 1, 2. Poultry Science, 90(2): 494–497. https://doi.org/10.3382/ps.2010-00891 Robyn, J., Rasschaert, G., Hermans, D., Pasmans, F. & Heyndrickx, M. 2013. Is allicin able to reduce Campylobacter jejuni colonization in broilers when added to drinking water? Poultry Science, 92(5): 1408–1418. https://doi. org/10.3382/ps.2012-02863 Sparks, N.H.C. 2009. The role of the water supply system in the infection and control of Campylobacter in chicken. World’s Poultry Science Journal, 65(3): 459–474. https://doi.org/10.1017/S0043933909000324 Szott, V., Peh, E., Friese, A., Roesler, U., Kehrenberg, C., Ploetz, M. & Kittler, S. 2022. Antimicrobial effect of a drinking water additive comprising four organic acids on Campylobacter load in broilers and monitoring of bacterial susceptibility. Poultry Science, 101(12): 102209. https://doi. org/10.1016/j.psj.2022.102209 CHAPTER 7 – ANNEX 87 Other additives and combination of additives Froebel, L.K., Jalukar, S., Lavergne, T.A., Coufal, C.D. & Duong, T. 2020. Administration of direct-fed Bacillus cultures and refined functional carbohydrates to broiler chickens improves growth performance and promotes positive shifts in gastrointestinal microbiota. Journal of Applied Poultry Research, 29(4): 765–774. https://doi.org/10.1016/ j.japr.2020.06.004 Greene, G., Koolman, L., Whyte, P., Lynch, H., Coffey, A., Lucey, B., Egan, J., O’Connor, L. & Bolton, D. 2022. The efficacy of organic acid, medium chain fatty acid and essential oil based broiler treatments; in vitro anti‐ Campylobacter jejuni activity and the effect of these chemical‐based treatments on broiler performance. Journal of Applied Microbiology, 132(1): 687–695. https://doi.org/10.1111/jam.15204 Grilli, E., Vitari, F., Domeneghini, C., Palmonari, A., Tosi, G., Fantinati, P., Massi, P. & Piva, A. 2013. Development of a feed additive to reduce caecal Campylobacter jejuni in broilers at slaughter age: from in vitro to in vivo , a proof of concept. Journal of Applied Microbiology, 114(2): 308–317. https://doi.org/10.1111/jam.12053 Wilson, K.M., Bourassa, D.V., McLendon, B.L., Wilson, J.L. & Buhr, R.J. 2018. Impact of skip-a-day and every-day feeding programs for broiler breeder pullets on the recovery of Salmonella and Campylobacter following challenge. Poultry Science, 97(8): 2775–2784. https://doi.org/10.3382/ps/ pey150 A4.2 Processing A total of 141 studies were reviewed by the processing group, including primary studies, reviews, and risk assessments that evaluated the efficiency of interventions implemented during poultry processing for Campylobacter control. Al-Qadiri, H.M., Ovissipour, M., Al-Alami, N., Govindan, B.N., Shiroodi, S.G. & Rasco, B. 2016. Efficacy of neutral electrolyzed water, quaternary ammonium and lactic acid‐based solutions in controlling microbial contamination of food cutting boards using a manual spraying technique. Journal of Food Science, 81(5). 88 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Bai, Y., Ding, X., Zhao, Q., Sun, H., Li, T., Li, Z., Wang, H. et al. 2022. Development of an organic acid compound disinfectant to control food- borne pathogens and its application in chicken slaughterhouses. Poultry Science, 101(6): 101842. https://doi.org/10.1016/j.psj.2022.101842 Bailey, M.A., Taylor, R.M., Brar, J.S., Corkran, S.C., Velásquez, C., Novoa Rama, E., Oliver, H.F. & Singh, M. 2019. Prevalence and antimicrobial resistance of Campylobacter from antibiotic-free broilers during organic and conventional processing. Poultry Science, 98(3): 1447–1454. https:// doi.org/10.3382/ps/pey486 Balta, I., Linton, M., Pinkerton, L., Kelly, C., Ward, P., Stef, L., Pet, I. et al. 2021. The effect of natural antimicrobials on the Campylobacter coli T6SS+/− during in vitro infection assays and on their ability to adhere to chicken skin and carcasses. 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The effect of chilling in cold air or ice water on the microbiological quality of broiler carcasses and the population of Campylobacter. Poultry Science, 87(5): 992–998. https://doi.org/10.3382/ps.2007-00406 Berrang, M.E., Windham, W.R. & Meinersmann, R.J. 2011. Campylobacter, Salmonella, and Escherichia coli on broiler carcasses subjected to a high pH scald and low pH postpick chlorine dip. Poultry Science, 90(4): 896– 900. https://doi.org/10.3382/ps.2010-00900 Bertram, R., Kehrenberg, C., Seinige, D. & Krischek, C. 2019. Peracetic acid reduces Campylobacter spp. numbers and total viable counts on broiler breast muscle and drumstick skins during modified atmosphere package storage. Poultry Science, 98(10): 5064–5073. https://doi.org/10.3382/ps/pez266 CHAPTER 7 – ANNEX 89 Birk, T., Grønlund, A.C., Christensen, B.B., Knøchel, S., Lohse, K. & Rosenquist, H. 2010. Effect of organic acids and marination ingredients on the survival of Campylobacter jejuni on Meat. Journal of Food Protection, 73(2): 258–265. https://doi.org/10.4315/0362-028X-73.2.258 Bourassa, D.V., Harris, C.E., Bartenfeld Josselson, L.N. & Buhr, R.J. 2021. Assessment of stabilized hydrogen peroxide for use in reducing Campylobacter levels and prevalence on broiler chicken wings. Journal of Food Protection, 84(3): 449–455. https://doi.org/10.4315/JFP-20-356 Boysen, L. & Rosenquist, H. 2009. Reduction of thermotolerant Campylobacter species on broiler carcasses following physical decontamination at slaughter. Journal of Food Protection, 72(3): 497–502. https://doi.org/10. 4315/0362-028X-72.3.497 Bucher, O., Waddell, L., Greig, J. & Smith, B.A. 2015. Systematic review-meta- analysis of the effect of chilling on Campylobacter spp. during primary processing of broilers. Food Control, 56: 211–217. https://doi.org/10.1016/ j.foodcont.2015.03.032 Burfoot, D. & Mulvey, E. 2011. Reducing microbial counts on chicken and turkey carcasses using lactic acid. 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Application of peroxyacetic acid for decontamination of raw poultry products and comparison to other commonly used chemical antimicrobial interventions: A review. Journal of Food Protection, 84(10): 1772–1783. https://doi.org/10.4315/JFP-21- 107 90 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Casagrande Proietti, P., Pergola, S., Bellucci, S., Menchetti, L., Miraglia, D. & Franciosini, M.P. 2018. Occurrence and antimicrobial susceptibility of Campylobacter spp. on fresh and refrigerated chicken meat products in Central Italy. Poultry Science, 97(8): 2895–2901. https://doi.org/10.3382/ ps/pey147 Chaine, A., Arnaud, E., Kondjoyan, A., Collignan, A. & Sarter, S. 2013. Effect of steam and lactic acid treatments on the survival of Salmonella Enteritidis and Campylobacter jejuni inoculated on chicken skin. 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Bio-mapping indicators and pathogen loads in a commercial broiler processing facility operating with high and low antimicrobial intervention levels. Foods, 11(6): 775. https://doi.org/10.3390/foods11060775 Deblais, L., Helmy, Y.A., Kumar, A., Antwi, J., Kathayat, D., Acuna, U.M., Huang, H. et al. 2019. Novel narrow spectrum benzyl thiophene sulfonamide derivatives to control Campylobacter. The Journal of Antibiotics, 72(7): 555–565. https://doi.org/10.1038/s41429-019-0168-x Dirks, B.P., Dobrynin, D., Fridman, G., Mukhin, Y., Fridman, A. & Quinlan, J.J. 2012. Treatment of raw poultry with nonthermal dielectric barrier discharge plasma to reduce Campylobacter jejuni and Salmonella enterica. Journal of Food Protection, 75(1): 22–28. https://doi.org/10.4315/0362- 028X.JFP-11-153 CHAPTER 7 – ANNEX 91 Dittoe, D.K., Feye, K.M., Peyton, B., Worlie, D., Draper, M.J. & Ricke, S.C. 2019. The addition of ViriditecTM Aqueous ozone to peracetic acid as an antimicrobial spray increases air quality while maintaining Salmonella Typhimurium, non-pathogenic Escherichia coli, and Campylobacter jejuni reduction on whole carcasses. Frontiers in Microbiology, 9: 3180. https:// doi.org/10.3389/fmicb.2018.03180 Dogan, O.B., Aditya, A., Ortuzar, J., Clarke, J. & Wang, B. 2022. A systematic review and meta‐analysis of the efficacy of processing stages and interventions for controlling Campylobacter contamination during broiler chicken processing. Comprehensive Reviews in Food Science and Food Safety, 21(1): 227–271. https://doi.org/10.1111/1541-4337.12860 Dogan, O.B., Clarke, J., Mattos, F. & Wang, B. 2019. A quantitative microbial risk assessment model of Campylobacter in broiler chickens: Evaluating processing interventions. Food Control, 100: 97–110. https://doi. org/10.1016/j.foodcont.2019.01.003 Duc, V.M., Kakiuchi, R., Obi, T., Asakura, H. & Chuma, T. 2022. The incidence of Campylobacter contamination levels through chicken-sashimi processing steps in a small-scale poultry processing plant applying the external stripping method. Journal of Veterinary Medical Science, 84(3): 414–419. https://doi.org/10.1292/jvms.21-0486 Duffy, L.L., Osmond-McLeod, M.J., Judy, J. & King, T. 2018. Investigation into the antibacterial activity of silver, zinc oxide and copper oxide nanoparticles against poultry-relevant isolates of Salmonella and Campylobacter. Food Control, 92: 293–300. https://doi.org/10.1016/ j.foodcont.2018.05.008 Ellerbroek, L.I., Lienau, J. ‐A. & Klein, G. 2010. Campylobacter spp. in broiler flocks at farm level and the potential for cross‐contamination during slaughter. Zoonoses and Public Health, 57(7–8). https://doi.org/10.1111/ j.1863-2378.2009.01267.x Erega, A., Stefanic, P., Dogsa, I., Danevčič, T., Simunovic, K., Klančnik, A., Smole Možina, S. & Mandic Mulec, I. 2021. Bacillaene mediates the inhibitory effect of bacillus subtilis on Campylobacter jejuni biofilms. Applied and Environmental Microbiology, 87(12): e02955-20. https://doi. org/10.1128/AEM.02955-20 92 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Figueroa, G., Troncoso, M., López, C., Rivas, P. & Toro, M. 2009. Occurrence and enumeration of Campylobacter spp. during the processing of Chilean broilers. BMC Microbiology, 9(1): 94. https://doi.org/10.1186/1471-2180-9-94 Foddai, A., Takeuchi-Storm, N., Høg, B.B., Kjeldgaard, J.S., Andersen, J.K. & Ellis-Iversen, J. 2022. Assessing Campylobacter cross-contamination of Danish broiler flocks at slaughterhouses considering true flock prevalence estimates and ad-hoc sampling. Microbial Risk Analysis, 21: 100214. https://doi.org/10.1016/j.mran.2022.100214 Franz, E., Van Der Fels-Klerx, H.J., Thissen, J. & Van Asselt, E.D. 2012. 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Foodborne Pathogens and Disease, 8(1): 109–117. Haydar Ozdemir, G.I.C., Gorkem Cengiz, B.O. & Sen, E. 2019. Effect of lactic acid and steam treatments on Campylobacter jejuni on chicken skin. Emirates Journal of Food and Agriculture: 143. https://doi.org/10.9755/ ejfa.2019.v31.i2.1915 94 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Horiuchi, I., Kawata, H., Nagao, T., Imaohji, H., Murakami, K., Kino, Y., Yamasaki, H. et al. 2015. Antimicrobial activity and stability of weakly acidified chlorous acid water. Biocontrol Science, 20(1): 43–51. https://doi. org/10.4265/bio.20.43 Hovorková, P. & Skřivanová, E. 2015. Use of caprylic acid in broiler chickens: effect on Campylobacter jejuni. Foodborne Pathogens and Disease, 12(8): 712–718. https://doi.org/10.1089/fpd.2015.1978 Huang, J., Zang, X., Zhai, W., Guan, C., Lei, T. & Jiao, X. 2017. Quantitative analysis of Campylobacter spp. contamination in chicken slaughtering lines by “label tracking method” in eastern China. Food Control, 80: 67–73. https://doi.org/10.1016/j.foodcont.2017.03.052 Iannetti, S., Calistri, P., Di Serafino, G., Marotta, F., Alessiani, A., Antoci, S., Neri, D. et al. 2020. Campylobacter jejuni and Campylobacter coli: prevalence, contamination levels, genetic diversity and antibiotic resistance in Italy. Veterinaria Italiana, 56(1). https://doi.org/10.12834/ VetIt.1819.9596 Isohanni, P., Alter, T., Saris, P. & Lyhs, U. 2010. Wines as possible meat marinade ingredients possess antimicrobial potential against Campylobacter. Poultry Science, 89(12): 2704–2710. https://doi.org/10.3382/ps.2009- 00521 Isohanni, P.M.I. & Lyhs, U. 2009. Use of ultraviolet irradiation to reduce Campylobacter jejuni on broiler meat. Poultry Science, 88(3): 661–668. https://doi.org/10.3382/ps.2008-00259 Ivanova, M., Singh, R., Dharmasena, M., Gong, C., Krastanov, A. & Jiang, X. 2014. Rapid identification of Campylobacter jejuni from poultry carcasses and slaughtering environment samples by real-time PCR. Poultry Science, 93(6): 1587–1597. https://doi.org/10.3382/ps.2013-03736 Jackowska-Tracz, A. & Tracz, M. 2015. Effects of high hydrostatic pressure on Campylobacter jejuni in poultry meat. Polish Journal of Veterinary Sciences, 18(2): 261–266. https://doi.org/10.1515/pjvs-2015-0034 Jiang, W., Li, K., Chiu, Y.-C., Waldman, C. & Shen, C. 2020. Inactivation of Campylobacter jejuni in moisture enhanced non-intact chicken patties by double pan-broiling as affected by cooking set-up temperature and pump rate. LWT, 133: 109938. https://doi.org/10.1016/j.lwt.2020.109938 CHAPTER 7 – ANNEX 95 Kameyama, M., Chuma, T., Nishimoto, T., Oniki, H., Yanagitani, Y., Kanetou, R., Gotou, K. et al. 2012. Effect of cooled and chlorinated chiller water on Campylobacter and coliform counts on broiler Carcasses during chilling at a middle-size poultry processing plant. Journal of Veterinary Medical Science, 74(1): 129–133. https://doi.org/10.1292/jvms.11-0167 Kataria, J., Vaddu, S., Rama, E.N., Sidhu, G., Thippareddi, H. & Singh, M. 2020. Evaluating the efficacy of peracetic acid on Salmonella and Campylobacter on chicken wings at various pH levels. Poultry Science, 99(10): 5137–5142. https://doi.org/10.1016/j.psj.2020.06.070 Koolman, L., Whyte, P., Meade, J., Lyng, J. & Bolton, D. 2014a. A Combination of chemical and ultrasonication treatments to reduce Campylobacter jejuni on raw poultry. Food and Bioprocess Technology, 7(12): 3602–3607. https://doi.org/10.1007/s11947-014-1370-2 Koolman, L., Whyte, P., Meade, J., Lyng, J. & Bolton, D. 2014b. Use of chemical treatments applied alone and in combination to reduce Campylobacter on raw poultry. Food Control, 46: 299–303. https://doi.org/10.1016/ j.foodcont.2014.05.041 Kottawatta, K., Van Bergen, M., Abeynayake, P., Wagenaar, J., Veldman, K. & Kalupahana, R. 2017. Campylobacter in broiler chicken and broiler meat in Sri Lanka: influence of semi-automated vs. wet market processing on Campylobacter contamination of broiler neck skin samples. Foods, 6(12): 105. https://doi.org/10.3390/foods6120105 Kumar, S., Singh, M., Cosby, D.E., Cox, N.A. & Thippareddi, H. 2020. Efficacy of peroxy acetic acid in reducing Salmonella and Campylobacter spp. populations on chicken breast fillets. Poultry Science, 99(5): 2655–2661. https://doi.org/10.1016/j.psj.2019.12.045 Kure, C.F., Axelsson, L., Carlehög, M., Måge, I., Jensen, M.R. & Holck, A. 2020. The effects of a pilot-scale steam decontamination system on the hygiene and sensory quality of chicken carcasses. Food Control, 109: 106948. https://doi.org/10.1016/j.foodcont.2019.106948 Lake, R.J., Horn, B.J., Dunn, A.H., Parris, R., Green, F.T. & McNickle, D.C. 2013. Cost-effectiveness of interventions to control Campylobacter in the New Zealand poultry meat food supply. Journal of Food Protection, 76(7): 1161–1167. https://doi.org/10.4315/0362-028X.JFP-12-481 96 MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT Landrum, M.A., Cox, N.A., Cosby, D.E., Berrang, M.E., Mize, S.C. & Jackson, J.S. 2017. 879 reduction of Campylobacter on chicken livers using a low- acid processing aid. Journal of Animal Science, 95(suppl_4): 377–377. https://doi.org/10.2527/asasann.2017.879 Lecompte, J.-Y., Collignan, A., Sarter, S., Cardinale, E. & Kondjoyan, A. 2009. Decontamination of chicken skin surfaces inoculated with Listeria innocua , Salmonella enteritidis and Campylobacter jejuni by contact with a concentrated lactic acid solution. British Poultry Science, 50(3): 307– 317. https://doi.org/10.1080/00071660902942742 Lee, N.-K., Jung, B.S., Na, D.S., Yu, H.H., Kim, J.-S. & Paik, H.-D. 2016. The impact of antimicrobial effect of chestnut inner shell extracts against Campylobacter jejuni in chicken meat. LWT - Food Science and Technology, 65: 746–750. https://doi.org/10.1016/j.lwt.2015.09.004 Liu, Y., Betti, M. & Gänzle, M.G. 2012. High pressure inactivation of Escherichia coli, Campylobacter jejuni, and spoilage microbiota on poultry meat. Journal of Food Protection, 75(3): 497–503. https://doi.org/10.4315/0362- 028X.JFP-11-316 Luning, P.A., Jacxsens, L., Rovira, J., Osés, S.M., Uyttendaele, M. & Marcelis, W.J. 2011. A concurrent diagnosis of microbiological food safety output and food safety management system performance: Cases from meat processing industries. Food Control, 22(3–4): 555–565. https://doi. org/10.1016/j.foodcont.2010.10.003 McWhorter, A.R., Weerasooriya, G., Willson, N.-L. & Chousalkar, K.K. 2022. Peroxyacetic acid and acidified sodium chlorite reduce microbial contamination on whole chicken carcasses obtained from two processing points. Food Microbiology, 106: 104035. https://doi.org/10.1016/ j.fm.2022.104035 Melero, B., Vinuesa, R., Diez, A.M., Jaime, I. & Rovira, J. 2013. Application of protective cultures against Listeria monocytogenes and Campylobacter jejuni in chicken products packaged under modified atmosphere. Poultry Science, 92(4): 1108–1116. https://doi.org/10.3382/ps.2012-02539 Meredith, H., McDowell, D. & Bolton, D.J. 2013. An evaluation of trisodium phosphate, citric acid and lactic acid cloacal wash treatments to reduce Campylobacter, total viable counts (TVC) and total enterobacteriaceae counts (TEC) on broiler carcasses during processing. Food Control, 32(1): 149–152. https://doi.org/10.1016/j.foodcont.2012.11.026 CHAPTER 7 – ANNEX 97 Meredith, H., Walsh, D., McDowell, D.A. & Bolton, D.J. 2013. An investigation of the immediate and storage effects of chemical treatments on Campylobacter and sensory characteristics of poultry meat. International Journal of Food Microbiology, 166(2): 309–315. https://doi.org/10.1016/ j.ijfoodmicro. 2013.07.005 Moazzami, M., Bergenkvist, E., FernströM, L.-L., Rydén, J. & Hansson, I. 2021. Reducing Campylobacter jejuni, Enterobacteriaceae, Escherichia coli, and total aerobic bacteria on broiler carcasses using combined ultrasound and steam. Journal of Food Protection, 84(4): 572–578. https://doi. org/10.4315/JFP-20-395 Moore, A., Nannapaneni, R., Kiess, A. & Sharma, C.S. 2017. Evaluation of USDA approved antimicrobials on the reduction of Salmonella and Campylobacter in ground chicken frames and their effect on meat quality. Poultry Science, 96(7): 2385–2392. https://doi.org/10.3382/ps/pew497 Morgan, R.B., Sierra–Arguello, Y.M., Perdoncini, G., Borges, K.A., Furian, T.Q., Gomes, M.J.P., Lima, D. et al. 2022. Comparison of transport crates contamination with Campylobacter spp. before and after the cleaning and disinfection procedure in broiler slaughterhouses. 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Shiga toxin-producing Escherichia coli (STEC) and food: attribution, characterization, and monitoring. 32 FAO and WHO. 2019. Attributing illness caused by Shiga toxin-producing Escherichia coli (STEC) to specific foods: report. MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT110 33 FAO and WHO. 2019. Safety and quality of water used in food production and processing: meeting report. 34 FAO and WHO. 2019. Foodborne antimicrobial resistance: role of the environment, crops and biocides: meeting report. 35 FAO and WHO. 2021. Advances in science and risk assessment tools for Vibrio parahaemolyticus and V. vulnificus associated with seafood: meeting report. 36 FAO and WHO. 2021. Microbiological risk assessment guidance for food: guidance. 37 FAO and WHO. 2021. Safety and quality of water used with fresh fruits and vegetables. 38 FAO and WHO. 2022. 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MEASURES FOR THE CONTROL OF CAMPYLOBACTER SPP. IN CHICKEN MEAT112 To collate and assess the most recent scientific information relevant to the control of thermotolerant Campylobacter species in broiler production and chicken meat, the Joint FAO/WHO Expert Meeting on Microbiological Risk Assessment (JEMRA) convened a meeting in Rome, Italy in February 2023. The expert committee reviewed the available data on Campylobacter control including scientific literature published from 2008 to October 2022 and data submitted in response to a call for data for this meeting. The experts: 1) determined the quality and quantity of evidence of control measures for Campylobacter, 2) evaluated the impact of measures to control Campylobacter in the broiler production chain, 3) determined which hazard-based interventions pertained specifically to Campylobacter and which were general to the control of foodborne pathogens in the pre- and post-harvest broiler production chain, and 4) reviewed and recommended revisions to the Guidelines for the Control of Campylobacter and Salmonella in Chicken Meat. This report describes the output of this expert meeting and the advice herein is useful for both risk assessors and risk managers, at national and international levels and those in the food industry working to control the hazard in poultry. Food Systems and Food Safety - Economic and Social Development jemra@fao.org http://www.fao.org/food-safety Food and Agriculture Organization of the United Nations Viale delle Terme di Caracalla 00153 Rome, Italy Department of Nutrition and Food Safety jemra@who.int www.who.int/health-topics/food-safety/ World Health Organization 20 Avenue Appia 1211 Geneva 27, Switzerland CC9607EN/1/03.24 ISBN 978-92-5-138584-5 ISSN 1726-5274 9 7 8 9 2 5 1 3 8 5 8 4 5