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Campylobacter in Chicken Meat

  • International Commission on Microbiological Specifications for Foods (ICMSF)
Chapter

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.

References

  1. ACMF (Australian Chicken Meat Federation). (2013). http://www.chicken.org.au/page.php?id=12. Accessed 22 Nov 2015.
  2. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. Allos, B. M. (2001). Campylobacter jejuni infections: Update on emerging issues and trends. Clinical Infectious Diseases, 32, 1201–1206.CrossRefPubMedGoogle Scholar
  5. Audits International. (2000). 1999 U.S. Food Temperature Evaluation. http://foodrisk.org/default/assets/File/Audits-FDA_temp_study.pdf. Accessed 16 Nov 2015.
  6. 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.Google Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.Google Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. 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.
  17. 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.
  18. 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.CrossRefPubMedGoogle Scholar
  19. 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.Google Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.Google Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.Google Scholar
  26. 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.CrossRefPubMedGoogle Scholar
  27. 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.
  28. 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.Google Scholar
  29. 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.
  30. 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.Google Scholar
  31. 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.
  32. 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.Google Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefPubMedGoogle Scholar
  36. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.
  43. 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.CrossRefPubMedGoogle Scholar
  44. 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.
  45. 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.CrossRefPubMedGoogle Scholar
  46. 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.CrossRefPubMedGoogle Scholar
  47. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Luber, P., & Bartelt, E. (2007). Enumeration of Campylobacter spp. on the surface and within chicken breast fillets. Journal of Applied Microbiology, 102, 313–318.CrossRefPubMedGoogle Scholar
  49. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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.CrossRefPubMedGoogle Scholar
  51. 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.CrossRefPubMedGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. Nauta, M. J. (2005). Microbiological risk assessment models for partitioning and mixing during food handling. International Journal of Food Microbiology, 100, 311–322.CrossRefPubMedGoogle Scholar
  54. 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.CrossRefGoogle Scholar
  55. 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.CrossRefPubMedGoogle Scholar
  56. Neill, D. S., Campbell, J. N., & Greene, J. A. (1984). Campylobacter species in broiler chickens. Avian Pathology, 13, 777–785.CrossRefPubMedGoogle Scholar
  57. Newell, D. G., & Fearley, C. (2003). Sources of Campylobacter colonization in chicken chickens. Applied and Environmental Microbiology, 69, 4343–4351.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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.CrossRefPubMedGoogle Scholar
  59. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 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.CrossRefGoogle Scholar
  61. 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.CrossRefPubMedGoogle Scholar
  62. 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.CrossRefPubMedGoogle Scholar
  63. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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.
  65. 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.CrossRefPubMedGoogle Scholar
  66. 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.CrossRefPubMedGoogle Scholar
  67. 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.
  68. 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.CrossRefPubMedGoogle Scholar
  69. 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.CrossRefPubMedGoogle Scholar
  70. 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.CrossRefPubMedGoogle Scholar
  71. 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.CrossRefPubMedGoogle Scholar
  72. 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.CrossRefPubMedGoogle Scholar
  73. Zwietering, M. (2005). Practical considerations on food safety objectives. Food Control, 16, 817–823.CrossRefGoogle Scholar

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© Springer International Publishing AG 2018

Authors and Affiliations

  • International Commission on Microbiological Specifications for Foods (ICMSF)
    • 1
  1. 1.Robert L. Buchanan, editorial committee chairRiverside Corporate Park CSIRONorth RydeAustralia

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