Abstract
The global trade in chicken meat is extensive. In 2016 world-wide imports totalled 8.9 million tons and world-wide exports totalled 10.8 million tons. Brazil is the largest exporter of chicken meat in the world at 4.1 million ton per annum in 2016 (USDA 2016). Production of chicken meat starts at the hatchery where chicks are reared. These are stocked into chicken farms where they are grown to the required weight. Chicken production farms range from organic operations which are committed to “free range rearing to intensive, enclosed chicken houses where birds are ready for slaughter at around 5–7 weeks of age. The ensuing processing stages of slaughter, dressing and chilling are highly mechanized with line processing speeds approaching 175 birds per min. This is followed by distribution and retail sale under chill or frozen conditions. There are many opportunities during primary production and processing for chickens and chicken meat to become infected with pathogenic bacteria. Salmonella and Campylobacter are the principle pathogens of concern, with the latter being the focus of this chapter.
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Notes
- 1.
“Intervals recorded as <10 cfu/g were set at 1 cfu/g and >10,000 cfu/g were set at 50,000 cfu/g before log10 transformation. The mid-point value of the interval was used for the X, P proportions of the cumulative data which were fitting to a normal distribution using @Risk™.”
- 2.
“Counts recorded as <10 cfu/g were set at 1 cfu/g before log10 transformation and fitting to a normal distribution using @Risk™”
- 3.
Based on a population 299 million for the U.S. (Scallan et al. 2011)
- 4.
Campylobacter level = 1.495 log10 cfu/g chicken, therefore 988 g of meat and skin would contain 30,886 Campylobacter cfu. If all on skin then log10(30,886/85) = 2.5603 log10 cfu/g skin or log10(30,886/100) = 2.4897 log10 cfu/ml carcass rinse water.
References
ACMF (Australian Chicken Meat Federation). (2013). http://www.chicken.org.au/page.php?id=12. Accessed 22 Nov 2015.
Agunos, A., Waddell, L., Leger, D., & Taboada, E. (2014). A systematic review characterizing on-farm sources of Campylobacter spp. for chicken chickens. PLoS One, 9, e104905. https://doi.org/10.1371/journal.pone.0104905.
Allen, V. M., Weaver, H., & Ridley, A. M. (2008). Sources and spread of thermophilic Campylobacter during partial depopulation of chicken flocks. Journal of Food Protection, 71, 264–270.
Allos, B. M. (2001). Campylobacter jejuni infections: Update on emerging issues and trends. Clinical Infectious Diseases, 32, 1201–1206.
Audits International. (2000). 1999 U.S. Food Temperature Evaluation. http://foodrisk.org/default/assets/File/Audits-FDA_temp_study.pdf. Accessed 16 Nov 2015.
Australian Government. (2012). Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of the OzFoodNet network, 2010. Communicable Diseases Intelligence, 36, E213–E241.
Bang, D. D., Nielsen, E. M., Scheutz, F., Pedersen, K., Handberg, K., & Madsen, M. (2003). PCR detection of seven virulence and toxin genes of Campylobacter jejuni and Campylobacter coli isolates from Danish pigs and cattle and cytolethal distending toxin production of the isolates. Journal of Applied Microbiology, 94, 1003–1014.
Bergsma, N. J., Fischer, A. R. H., van Asselt, E. D., Zwietering, M. H., & de Jong, A. E. I. (2007). Consumer food preparation and its implication for survival of Campylobacter jejuni on chicken. British Food Journal, 109, 548–561.
Bashor, M. P., Curtis, P. A., Keener, K. M., Sheldon, B. W., Kathariou, S., & Osborne, J. A. (2004). Effects of carcass washers on Campylobacter contamination in large broiler processing plants. Poultry Science, 83, 1232–1239.
Black, R. E., Levine, M. M., Clements, M. L., Hughes, T. P., & Blaser, M. J. (1988). Experimental Campylobacter jejuni infection in humans. The Journal of Infectious Diseases, 157, 472–479.
Bull, S. A., Allen, V. M., Domingue, G., Jørgensen, F., Frost, J. A., Ure, R., Whyte, R., Tinker, D., Corry, J. E., Gillard-King, J., & Humphrey, T. J. (2006). Sources of Campylobacter spp. colonizing housed chicken flocks during rearing. Applied and Environmental Microbiology, 72, 645–652.
Bull, S. A., Thomas, A., Humphrey, T., Ellis-Iversen, J., Cook, A. J., Lovell, R., & Jorgensen, F. (2008). Flock health indicators and Campylobacter spp. in commercial housed chickens reared in great Britain. Applied and Environmental Microbiology, 74, 5408–5413.
Byrd, J. A., Sams, A. R., Hargis, B. M., & Caldwell, D. J. (2011). Effect of selected modified atmosphere packaging on Campylobacter survival in raw poultry. Poultry Science, 90, 1324–1328. https://doi.org/10.3382/ps.2010-00746.
CDC (Centers for Disease Control and Prevention). (2013). Incidence and trends of infection with pathogens transmitted commonly through food — Foodborne diseases active surveillance network, 10 U.S. sites, 2006–2013. Morbidity and Mortality Weekly Report, 63, 328–332.
Chuma, T., Hashimoto, S., & Okamoto, K. (2000). Detection of thermophilic campylobacters from sparrows by multiplex PCR: The role of sparrows as a source of contamination of chickens with Campylobacter. The Journal of Veterinary Medical Science, 62, 1291–1295.
Codex Alimentarius Commission. (2007). Principles and guidelines for the conduct of microbiological risk management. CAC/GL 63–2007. www.codexalimentarius.org/download/standards/10740/CXG_061e.pdf. Accessed 24 Sept 2015.
Codex Alimentarius Commission. (2011). Guidelines for the control of Campylobacter and Salmonella in chicken meat. CAC/GL 78–2011. http://www.fao.org/fao-who-codexalimentarius/sh-proxy/en/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FStandards%252FCAC%2BGL%2B78-2011%252FCXG_078e.pdf. Accessed 24 Oct 2015.
Datta, S., Niwa, H., & Itoh, K. (2003). Prevalence of 11 pathogenic genes of Campylobacter jejuni by PCR in strains isolated from humans, poultry meat and chicken and bovine faeces. Journal of Medical Microbiology, 52, 345–348. https://doi.org/10.1099/jmm.0.05056-0.
De Jong, A. E. I., van Asselt, E. D., Zwietering, M. H., Nauta, M. J., & de Jonge, R. (2012). Extreme heat resistance of food borne pathogens Campylobacter jejuni, Escherichia coli, and Salmonella Typhimurium on chicken breast fillet during cooking. Internet Journal of Microbiology, 2012, 196841. https://doi.org/10.1155/2012/196841.
Duffy, L. L., Blackall, P. J., Cobbold, R. N., & Fegand, N. (2014). Quantitative effects of in-line operations on Campylobacter and Escherichia coli through two Australian chicken processing plants. International Journal of Food Microbiology, 188, 128–134.
Edwards, D. S., Milne, L. M., Morrow, K., Sheridan, P., Verlander, N. Q., Mulla, R., Richardson, J. F., Pender, A., Lilley, M., & Reacher, M. (2014). Campylobacteriosis outbreak associated with consumption of undercooked chicken liver pâté in the east of England, September 2011: Identification of a dose–response risk. Epidemiology and Infection, 142, 352–357. https://doi.org/10.1017/S0950268813001222.
EFSA (European Food Safety Authority). (2010a). Scientific opinion on quantification of the risk posed by broiler meat to human campylobacteriosis in the EU. EFSA Journal, 8(1), 1437.
EFSA (European Food Safety Authority). (2010b). Analysis of the baseline survey on the prevalence of Campylobacter in chicken batches and of Campylobacter and Salmonella on chicken carcasses in the EU, 2008: Part a: Campylobacter and Salmonella prevalence estimates. EFSA Journal, 8(8), 1503.
EFSA (European Food Safety Authority). (2011). Scientific opinion on Campylobacter in chicken meat production: Control options and performance objectives and/or targets at different stages of the food chain. EFSA Journal, 9(4), 2105.
EFSA (European Food Safety Authority). (2015). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA Journal, 13(12), 4329.
Ellis-Iversen, J., Ridley, A., Morris, V., Sowa, A., Harris, J., Atterbury, R., Sparks, N., & Allen, V. (2012). Persistent environmental reservoirs on farms as risk factors for Campylobacter in commercial poultry. Epidemiology and Infection, 140, 916–924.
ESR (Institute of Environmental Science & Research Limited). (2007). Risk Profile: Campylobacter jejuni/coli in poultry (whole and pieces). Lake, R., Hudson, A., Cressey, P. & Gilbert, S. https://www.esr.cri.nz. Accessed 20 Oct 2014.
ESR (Environmental Science and Research Limited). (2011). Annual Report Concerning Foodborne Disease in New Zealand 2010. http://foodsafety.govt.nz/elibrary/industry/FBI-report-2011.pdf. Accessed 13 October 2014.
FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization). (2002). Risk assessments of Salmonella in eggs and chicken chickens. ftp://ftp.fao.org/docrep/fao/005/y4392e/y4392e00.pdf. Accessed 19 Oct 2014.
FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization). (2009). Risk assessments of Campylobacter spp. in chicken chickens: Technical Report. Microbiological Risk Assessment Series No 12. Geneva. 132pp.
FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization). (2008). Benefits and risks of using chlorine-containing disinfectants in food production and food processing. http://www.fao.org/docrep/012/i1357e/i1357e.pdf. Accessed 22 Feb 2016.
Fazil, A., Lowman, R., Stern, N. & Lammerding, A. (1999). Quantitative risk assessment model for Campylobacter jejuni in chicken. Abstracts of the 10th International Workshop on CHRO, Baltimore, MD, US p. 65.
Fernandes, M., Mena, C., Silva, I., & Teixeira, P. (2010). Study of cytolethal distending toxin (cdt) in Campylobacter coli using a multiplex polymerase chain reaction assay and its distribution among clinical and food strains. Foodborne Pathogens and Disease, 7, 103–106.
Georgsson, F., Thornorkelsson, A. E., Geirsdottira, M., Reiersenc, J., & Stern, N. J. (2006). The influence of freezing and duration of storage on Campylobacter and indicator bacteria in chicken carcasses. Food Microbiology, 23, 677–683.
Guerin, M. T., Sir, C., Sargeant, J. M., Waddell, L., O’Connor, A. M., Wills, R. W., Bailey, R. H., & Byrd, J. A. (2010). The change in prevalence of Campylobacter on chicken carcasses during processing: A systematic review. Poultry Science, 89, 1070–1084.
Hald, B., Skovgård, H., Bang, D. D., Pedersen, K., Dybdahl, J., Jespersen, J. B., & Madsen, M. (2004). Flies and Campylobacter infection of chicken flocks. Emerging Infectious Diseases, 10, 1490–1492.
Hartnett, E., Kelly, L., Newell, D., Wooldridge, M., & Gettinby, G. (2001). A quantitative risk assessment for the occurrence of Campylobacter in chickens at the point of slaughter. Epidemiology and Infection, 127, 195–206.
Haruna, M., Sasaki, Y., Murakami, M., Ikeda, A., Kusukawa, M., Tsujiyama, Y., Ito, K., Asai, T., & Yamada, Y. (2012). Prevalence and antimicrobial susceptibility of Campylobacter in chicken flocks in Japan. Zoonoses and Public Health, 59, 241–245.
Havelaar, A. H., Mangen, M. J. J., De Koeijer, A. A., Bogaardt, M. J., Evers, E. G., Jacobs-Reitsma, W. F., Van Pelt, W., Wagenaar, J. A., De Wit, G. A., Van der Zee, H., & Nauta, M. J. (2007). Effectiveness and efficiency of controlling Campylobacter on broiler chicken meat. Risk Analysis, 27, 831–844.
Hue, O., Le Bouquin, S., Laisney, M. J., Virginie, A., Lalande, F., Petetin, I., Rouxel, S., Quesne, S., Gloaguen, P.-Y., Picherot, M., Santolini, J., Salvat, G., Bougeard, S., & Chemaly, M. (2010). Prevalence of and risk factors for Campylobacter spp. contamination of chicken carcasses at the slaughterhouse. Food Microbiology, 27, 992–999.
Jamali, H., Ghaderpour, A., Radmehr, B., Chuan Wei, K. S., Chai, L. C., & Ismail, S. (2015). Prevalence and antimicrobial resistance of Campylobacter species isolates in ducks and geese. Food Control, 50, 328–330.
Jorgensen, F., Madden, R.H., Arnold, E., Charlett, A. & Elviss, N.C. (2015). A Microbiological survey of Campylobacter contamination in fresh whole UK produced chilled chickens at retail sale (2014–15). FSA Project FS241044 https://www.food.gov.uk/sites/default/files/campylobacter-retail-survey-final-report.pdf. Accessed 22 Nov 2015.
Koolman, L., Whyte, P., & Bolton, D. J. (2014). An investigation of broiler caecal Campylobacter counts at first and second thinning. Journal of Applied Microbiology, 117, 876–881.
Lake, R., Hudson, A., Cressey, P. & Bayne, G. (2007). Quantitative risk model: Campylobacter spp. in the poultry food chain. Report of the Institute of Environmental Science and Research Limited, Christchurch, New Zealand 1–91. http://www.foodsafety.govt.nz/elibrary/industry/Quantitative_Risk-Science_Research.pdf. Accessed 24 Oct 2016.
Lawes, J. R., Vidal, A., Clifton-Hadley, F. A., Sayers, R., Rodgers, J., Snow, L., Evans, S. J., & Powell, L. F. (2012). Investigation of prevalence and risk factors for Campylobacter in chicken flocks at slaughter: Results from a UK survey. Epidemiology and Infection, 140, 1725–1737. https://doi.org/10.1017/S0950268812000982.
Lindqvist, R., & Lindblad, M. (2008). Quantitative risk assessment of thermophilic Campylobacter spp. and cross-contamination during handling of raw broiler chickens evaluating strategies at the producer level to reduce human campylobacteriosis in Sweden. International Journal of Food Microbiology, 121, 41–52.
Luber, P., Brynestad, S., Topsch, D., Scherer, K., & Bartelt, E. (2006). Quantification of Campylobacter species cross-contamination during handling of contaminated fresh chicken parts in kitchens. Applied and Environmental Microbiology, 72, 66–70.
Luber, P., & Bartelt, E. (2007). Enumeration of Campylobacter spp. on the surface and within chicken breast fillets. Journal of Applied Microbiology, 102, 313–318.
Maziero, M. T., & de Oliveira, T. C. R. M. (2010). Effect of refrigeration and frozen storage on the Campylobacter jejuni recovery from naturally contaminated chicken carcasses. Brazilian Journal of Microbiology, 41, 501–505.
Meredith, H., Valdramidis, V., Rotabakk, B. T., Sivertsvik, M., McDowell, D., & Bolton, D. J. (2014). Effect of different modified atmospheric packaging (MAP) gaseous combinations on Campylobacter and the shelf-life of chilled poultry fillets. Food Microbiology, 44, 196–203.
Moreno, G. S., Griffiths, P. L., Connerton, I. F., & Park, R. W. (1993). Occurrence of campylobacters in small domestic and laboratory animals. The Journal of Applied Bacteriology, 75, 49–54.
NACMCF (U.S. National Advisory Committee for Microbiological Criteria for Foods). (2007). Response to the questions posed by the Food Safety and Inspection Service regarding consumer guidelines for the safe cooking of poultry products. Journal of Food Protection, 70, 251–260.
Nauta, M. J. (2005). Microbiological risk assessment models for partitioning and mixing during food handling. International Journal of Food Microbiology, 100, 311–322.
Nauta, M. J. (2007). Uncertainty and variability in predictive models of microorganisms in food. In S. Brul, S. Van Gerwen, & M. Zwietering (Eds.), Modelling microorganisms in food (pp. 44–66). Cambridge: Woodhead Publishing Ltd.
Nauta, M. J., Hill, A., Rosenquist, H., Brynestad, S., Fetsch, A., van der Logt, P., Fazil, A., Christensen, B., Katsma, K., Borck, B., & Havelaar, A. (2009). A comparison of risk assessments on Campylobacter in chicken meat. International Journal of Food Microbiology, 129, 107–123.
Neill, D. S., Campbell, J. N., & Greene, J. A. (1984). Campylobacter species in broiler chickens. Avian Pathology, 13, 777–785.
Newell, D. G., & Fearley, C. (2003). Sources of Campylobacter colonization in chicken chickens. Applied and Environmental Microbiology, 69, 4343–4351.
Oporto, B., Esteban, J. I., Aduriz, G., Juste, R. A., & Hurtado, A. (2007). Prevalence and strain diversity of thermophilic Campylobacter in cattle, sheep and swine farms. Journal of Applied Microbiology, 103, 977–984.
Pope, J. E., Krizova, A., Garg, A. X., Thiessen-Philbrook, H., & Ouimet, J. M. (2007). Campylobacter reactive arthritis: A systematic review. Seminars in Arthritis and Rheumatism, 37, 48–55.
Redmond, E. C., Griffith, C. J., Slader, J., & Humphry, T. J. (2004). Microbiological and observational analysis of cross contamination risks during domestic food preparation. British Food Journal, 106, 581–597.
Rosenquist, H., Nielsen, N. L., Sommer, H. M., Norrung, B., & Christensen, B. B. (2003). Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. International Journal of Food Microbiology, 83, 87–103.
Scanlon, K. A., Cagney, C., Walsh, D., McNulty, D., Carroll, A., McNamara, E. B., McDowell, D. A., & Duffy, G. (2013). Occurrence and characteristics of fastidious Campylobacteraceae species in porcine samples. International Journal of Food Microbiology, 163, 6–13.
Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. J., Jones, J. L., & Griffin, P. M. (2011). Foodborne illness acquired in the United States—Major pathogens. Emerging Infectious Diseases, 17, 7–15.
Silva, J., Leite, D., Fernandes, M., Mena, C., Gibbs, P. A., & Teixeira, P. (2011). Campylobacter spp. as a foodborne pathogen: A review. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2011.00200. Accessed 15 Oct 2016.
Sommer, H. M., Heuer, O. E., Sørensen, A. I. V., & Madsen, M. (2013). Analysis of factors important for the occurrence of Campylobacter in Danish chicken flocks. Preventive Veterinary Medicine, 111, 100–111.
Stern, N. J., Fedorka-Cray, P., Bailey, J. S., Cox, N. A., Craven, S. E., Hiett, K. L., Musgrove, M. T., Ladely, S., Cosby, D., & Mead, G. C. (2001). Distribution of Campylobacter spp. in selected U.S. poultry production and processing operations. Journal of Food Protection, 64, 1705–1710.
USDA (United States Department of Agriculture). (2016). Livestock and poultry: World markets and trade. http://apps.fas.usda.gov/psdonline/circulars/livestock_poultry.pdf. Accessed 24 Oct 20146.
Uyttendaele, M., Baert, K., Ghafir, Y., Daube, G., De Zutterm, L., Hermanm, L., Dierick, K., Pierard, D., Dubois, J. J., Horion, B., & Debevere, J. (2006). Quantitative risk assessment of Campylobacter spp. in poultry based meat preparations as one of the factors to support the development of risk-based microbiological criteria in Belgium. International Journal of Food Microbiology, 111, 149–163.
Van Asselt, E. D., & Zwietering, M. (2006). A systematic approach to determine global thermal inactivation parameters for various food pathogens. International Journal of Food Microbiology, 107(1), 73–82.
Wieczorek, K., Denis, E., Lynch, O., & Osek, J. (2013). Molecular characterization and antibiotic resistance profiling of Campylobacter isolated from cattle in polish slaughterhouses. Food Microbiology, 34, 130–136.
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, 238–241.
Yabe, S., Higuchi, W., Takano, T., Razvina, O., Iwao, Y., Isobe, H., & Yamamoto, T. (2010). In vitro susceptibility to antimicrobial agents and ultrastructural characteristics related to swimming motility and drug action in Campylobacter jejuni and C. coli. Journal of Infection and Chemotherapy, 16, 174–185.
Zwietering, M. (2005). Practical considerations on food safety objectives. Food Control, 16, 817–823.
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International Commission on Microbiological Specifications for Foods (ICMSF). (2018). Campylobacter in Chicken Meat. In: Microorganisms in Foods 7. Springer, Cham. https://doi.org/10.1007/978-3-319-68460-4_19
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