Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses, in the EU, 2008 - Part B: Analysis of factors associated with Campylobacter colonisation of broiler batches and with Campylobacter contamination of broiler carcasses; and investigation of the culture method diagnostic characteristics used to analyse broiler carcass samples

EFSA Journal

Volumn 8, Issue 8, 2010, Pages

[No Author Info available]

Author keywords

baseline survey; broiler batches; broiler carcasses; Campylobacter; chicken; EU; risk factors

Indexed keywords

EID: 85066047896     PISSN: None     EISSN: 18314732     Source Type: Journal    
DOI: 10.2903/j.efsa.2010.1522     Document Type: Article

References (72)

1. Aerts M, Geys H, Molenberghs G and Ryan L, 2002. Topics in Modelling of Clustered Data, Chapman and Hall, London.
2. Agresti A, 1996. An introduction to categorical data analysis, John Wiley and Sons.
3. Agresti A, 2002. Categorical data analysis, Wiley, Hoboken, New Jersey.
4. Allen VM, Bull SA, Corry JEL, Domingue G, Jørgensen F, Frost JA, Whyte R, Gonzalez A, Elviss N and Humphrey TJ, 2007. Campylobacter spp. contamination of chicken carcasses during processing in relation to flock colonisation, International Journal of Food Microbiology, 113, 54–61.
5. Allen VM, Weaver H, Ridley AM, Harris JA, Sharma M, Emery J, Sparks N, Lewis M and Edge S, 2008. Sources and spread of thermophilic Campylobacter spp. during partial depopulation of broiler chicken flocks, Journal of Food Protection, 71, 264–270.
6. Barrios PB, Reiersen J, Lowman R, Bisaillon J-R, Michel P, Fridriksdóttir V, Gunnarsson E, Stern N, Berke O, McEwen S and Martin W, 2006. Risk factors for Campylobacter spp. colonisation in broiler flocks in Iceland, Preventive Veterinary Medicine, 74, 264–278.
7. Berrang ME and Dickens JA, 2000. Presence and level of Campylobacter spp. on broiler carcasses throughout the processing plant, Journal of Applied Poultry Research, 9, 43–47.
8. Berrang ME, Buhr RJ, Cason JA and Dickens, JA, 2001. Broiler carcass contamination with Campylobacter from feces during defeathering, Journal of Food Protection, 64, 2063–2066.
9. Berrang ME and Dickens JA, 2004. The contribution of soiled surfaces within feather picking machines to Campylobacter counts on broiler carcasses. Journal of Applied Poultry Research, 13, 588–592.
10. Berrang ME, Northcutt JK and Dickens JA, 2004. The contribution of airborne contamination to Campylobacter counts on defeathered broiler carcasses, Journal of Applied Poultry Research, 13, 1–4.
11. Berndtson E, Emanuelson U, Engvall A and Danielsson-Tham ML, 1996. A 1-year epidemiological study of campylobacters in 18 Swedish chicken farms, Preventive Veterinary Medicine, 26, 167–185.
12. Best EL, Powell EJ, Swift C, Grant KA and Frost JA, 2003. Applicability of a rapid duplex real-time PCR assay for speciation of Campylobacter jejuni and Campylobacter coli directly from culture plates, FEMS Microbiology Letters, 229, 237–241.
13. Bouwknegt M, van den Giessen AW, Dam-Deisz WDC, Havelaar AH, Nagelkerke NJD and Henken AM, 2004. Risk factors for the presence of Campylobacter spp. in Dutch broiler flocks, Preventive Veterinary Medicine, 62, 35–49.
14. Bross IDJ, 1958. How to use Ridit analysis, Biometrics, 14, 18–38.
15. Bull SA, Allen VM, Domingue G, Jørgensen F, Frost JA, Ure R, Whyte R, Tinker D, Corry JE, Gillard-King J and Humphrey TJ, 2006. Sources of Campylobacter spp. colonising housed broiler flocks during rearing, Applied and Environmental Microbiology, 72, 645–52.
16. Callicott KA, Friethriksdóttir V, Reiersen J, Lowman R, Bisaillon JR, Gunnarsson E, Berndtson E, Hiett KL, Needleman DS and Stern NJ, 2006. Lack of evidence for vertical transmission of Campylobacter spp. in chickens, Applied and Environmental Microbiology, 72, 5794–5798.
17. Diggle PJ, Liang KY and Zeger SL, 1994. Analysis of longitudinal data, Oxford University Press, Oxford.
18. Diggle PJ, Heagerty PJ, Liang K-Y and Zeger SL, 2002. Analysis of longitudinal data, Second edition, Oxford Science Publications, Clarendon Press, Oxford.
19. Doorduyn Y, Van den Brandhof WE, Van Duynhoven, YT, Breukink BJ, Wagenaar JA and Van Pelt W, 2010. Risk factors for indigenous Campylobacter jejuni and Campylobacter coli infections in the Netherlands: a case-control study, Epidemiology and Infection, 1–14.
20. ECDC (European Centre for Disease Prevention and Control), 2008. Annual Epidemiological Report on Communicable Diseases in Europe 2008, Stockholm, European Centre for Disease Prevention and Control.
21. Edson DC, Empson S and Massey LD, 2009. Pathogen detection in food microbiology laboratories: an analysis of qualitative proficiency test data, 1999–2007, Journal of Food Safety, 29, 521–530.
22. EFSA (European Food Safety Authority), 2005. Opinion of the Scientific Panel on Biological Hazards on the request from the Commission related to Campylobacter in animals and foodstuffs, The EFSA Journal, 173, 1–10.
23. EFSA (European Food Safety Authority), 2007. Report of Task Force on Zoonoses Data Collection on proposed technical specifications for a coordinated monitoring programme for Salmonella and Campylobacter in broiler meat in the EU, The EFSA Journal, 92, 1–33.
24. EFSA (European Food Safety Authority), 2009a. Report of the Task Force on Zoonoses Data Collection on the statistical analysis of temporal and spatial trends of zoonotic agents in animals and food. Part I: critical review of the statistical analysis carried out on the Community Summary Report 2006 data, The EFSA Journal, 253, 1–77.
25. EFSA (European Food Safety Authority), 2009b. The Community Summary Report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and food-borne outbreaks in the European Union in 2007, The EFSA Journal, 223.
26. EFSA (European Food Safety Authority), 2009c. Assessing health benefits of controlling Campylobacter in the food chain. EFSA Scientific Colloquium Summary Report 12. 4–5 December 2008, Rome, Italy.
27. EFSA (European Food Safety Authority), 2010a. Report of Task Force on Zoonoses Data Collection on the analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Salmonella on broiler carcasses in the EU, 2008, Part A: Campylobacter and Salmonella prevalence estimates, The EFSA Journal, 8(03), 1503
28. EFSA (European Food Safety Authority) Panel on Biological Hazards (BIOHAZ), 2010b. Scientific Opinion on quantification of the risk posed by broiler meat to human campylobacteriosis in the EU. The EFSA Journal, 8(1), 1437.
29. EFSA (European Food Safety Authority), 2010c. The Community Summary Report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008, The EFSA Journal, 8(1), 1496.
30. El-Shibiny A, Connerton PL and Connerton IF, 2005. Enumeration and diversity of campylobacters and bacteriophages isolated during the rearing cycles of free-range and organic chickens, Applied and Environmental Microbiology, 71, 1259–1266.
31. Evans SJ and Sayers AR, 2000. A longitudinal study of Campylobacter infection of broiler flocks in Great Britain, Preventive Veterinary Medicine, 46, 209–223.
32. Gardner IA, 2004. An epidemiologic critique of current microbial risk assessment practice: the importance of prevalence and test accuracy, Journal of Food Protection, 67, 2000–2007.
33. Gillespie IA, O'Brien SJ, Frost JA, Adak GA, Horby P, Swan AV, Painter MJ, Neal KR and the Campylobacter Sentinel Surveillance Scheme Collaborators, 2002. A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses, Emerging Infectious Diseases, 8, 937–942.
34. Gregory E, Barnhart H, Dreesen DW, Stern NJ and Corn JL, 1997. Epidemiological study of Campylobacter spp. in broilers: source, time of colonisation, and prevalence, Avian Diseases, 41, 890–898.
35. Habib I, Sampers I, Uyttendaele M, De Zutter L and Berkvens D, 2008. A Bayesian modelling framework to estimate Campylobacter prevalence and culture methods sensitivity: application to a chicken meat survey in Belgium, Journal of Applied Microbiology, 105, 2002–2008.
36. Hald B, Rattenborg E and Madsen M, 2001. Role of batch depletion of broiler houses on the occurrence of Campylobacter spp. in chicken flocks, Letters in Applied Microbiology, 32, 253–6.
37. Hald B, Skovgård H, Pedersen K and Bunkenborg H, 2008. Influxed insects as vectors for Campylobacter jejuni and Campylobacter coli in Danish broiler houses, Poultry Science, 87, 1428–1434.
38. Hansson I, Ederoth M, Andersson L, Vågsholm I and Olsson Engvall E, 2005. Transmission of Campylobacter spp. to chickens during transport to slaughter, Journal of Applied Microbiology, 99, 1149–1157.
39. Hansson I, Forshell LP, Gustafsson P, Boqvist S, Lindblad J, Engvall EO, Andersson Y and Vågsholm I, 2007. Summary of the Swedish Campylobacter program in broilers, 2001 through 2005, Journal of Food Protection, 70, 2008–2014.
40. Hartnett E, Kelly L, Newell D, Wooldridge M and 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.
41. Heuer OE, Pedersen K, Andersen JS and Madsen M, 2001. Prevalence and antimicrobial susceptibility of thermophilic Campylobacter in organic and conventional broiler flocks, Letters in Applied Microbiology, 33, 269–274.
42. Hofshagen M and Kruse H, 2005. Reduction in flock prevalence of Campylobacter spp. in broilers in Norway after implementation of an action plan, Journal of Food Protection, 68, 2220–2223.
43. Huezo R, Northcutt JK, Smith DP, Fletcher DL and Ingram KD, 2007. Effect of dry air or immersion chilling on recovery of bacteria from broiler carcasses, Journal of Food Protection, 70, 1829–1834.
44. Humphrey TJ, Henley A and Lanning DG, 1993. The colonisation of broiler chickens with Campylobacter jejuni: some epidemiological investigations, Epidemiology and Infection, 110, 601–607
45. ISO (International Organization for Standardization), 2006a. Microbiology of food and animal feeding stuffs - Horizontal method for detection and enumeration of Campylobacter spp. - Part 1: Detection method. ISO 10272–1:2006.
46. ISO (International Organization for Standardization), 2006b. Microbiology of food and animal feeding stuffs - Horizontal method for detection and enumeration of Campylobacter spp. - Part 2: Colony-count technique. ISO/TS 10272–2:2006.
47. Jasson V, Sampers I, Botteldoorn N, López-Gálvez F, Baert L, Denayer S, Rajkovic A, Habib I, De Zutter L, Debevere J and Uyttendaele M, 2009. Characterization of Escherichia coli from raw poultry in Belgium and impact on the detection of Campylobacter jejuni using Bolton broth, International Journal of Food Microbiology, 135, 248–53.
48. Jore S, Viljugrein H, Brun E, Heier BT, Borck B, Ethelberg S, Hakkinen M, Kuusi M, Reiersen J, Hansson I, Engvall EO, Løfdahl M, Wagenaar JA, van Pelt W, Hofshagen M. 2010. Trends in Campylobacter incidence in broilers and humans in six European countries, 1997–2007, Preventive Veterinary Medicine 93(1):33–41. Epub 2009 Oct 17.
49. Johannessen GS, Johnsen G, Okland M, Cudjoe KS and Hofshagen M, 2007. Enumeration of thermotolerant Campylobacter spp. from poultry carcasses at the end of the slaughter-line, Letters in Applied Microbiology, 44, 92–97.
50. Lindqvist R and 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.
51. Lund MA, Welch TK, Griswold K, Endres JB and Sheperd C, 2003. Occurrence of Campylobacter and Salmonella in broiler chickens raised in different production systems and fed organic and traditional feed, Food Protection Trends, 23, 252–256.
52. Mantel N and Haenszel W, 1959. Statistical aspects of the analysis of data from retrospective studies of disease, Journal of the National Cancer Institute, 22, 719–748.
53. McCrea BA, Tonooka KH, VanWorth C, Boogs CL, Atwill ER and Schrader JS, 2006. Prevalence of Campylobacter and Salmonella species on farm, after transport, and at processing in specialty market poultry, Poultry Science, 85, 136–143.
54. Meeyam T, Padungtod P and Kaneene JB, 2004. Molecular characterization of Campylobacter isolated from chickens and humans in northern Thailand, Southeast Asian Journal of Tropical Medicine and Public Health, 35, 670–675.
55. Molenberghs G and Verbeke G, 2005. Models for discrete longitudinal data, Springer, New York.
56. Nadeau E, Messier S and Quessy S, 2002. Prevalence and comparison of genetic profiles of Campylobacter strains isolated from poultry and sporadic cases of campylobacteriosis in humans, Journal of Food Protection, 65, 73–78.
57. Nauta M, Hill A, Rosenquist H, Brynestad S, Fetsch A, van der Logt P, Fazil A, Christensen B, Katsma E, Borck B and Havelaar A, 2009. A comparison of risk assessments on Campylobacter in broiler meat, International Journal of Food Microbiology, 129, 107–123.
58. Neter J., Kutner MH, Nachtsheim CJ and Wasserman W, 1996. Applied linear statistical models, Fourth edition, McGraw-Hill.
59. Neuhaus JM, 1992. Statistical methods for longitudinal and clustered designs with binary responses, Statistical Methods in Medical Research, 1, 249–273.
60. Newell DG and Fearnley C, 2003. Sources of Campylobacter colonisation in broiler chickens, Applied and Environmental Microbiology, 69, 4343–4351.
61. Näther G, Alter T, Martin A and Ellerbroek L, 2009. Analysis of risk factors for Campylobacter species infection in broiler flocks, Poultry Science, 88, 1299–1305.
62. On SLW and Jordan PJ, 2003. Evaluation of 11 PCR assays for species level identification of Campylobacter jejuni and Campylobacter coli, Journal of Clinical Microbiology, 41, 330–336.
63. Padungtod P and Kaneene JB, 2005. Campylobacter in food animals and humans in northern Thailand, Journal of Food Protection, 68, 2519–2526.
64. Refrégier-Petton J, Rose N, Denis S and Salvat G, 2001. Risk factors for Campylobacter spp. contamination in French broiler-chicken flocks at the end of the rearing period, Preventive Veterinary Medicine, 50, 89–100.
65. Rosenquist H, Sommer HM, Nielsen NL and Christensen BB, 2006. The effect of slaughter operations on the contamination of chicken carcasses with thermotolerant Campylobacter, International Journal of Food Microbiology, 108, 226–232.
66. Russa AD, Bouma A, Vernooij JC, Jacobs-Reitsma W and Stegeman JA, 2005. No association between partial depopulation and Campylobacter spp. colonisation of Dutch broiler flocks, Letters in Applied Microbiology, 41, 280–285.
67. Skellam JG, 1948. A probability distribution derived from the binomial distribution by regarding the probability of success as variable between the sets of trials, Journal of the Royal Statistical Society, Series B, 10, 257–261.
68. Spearman C, 1904. The proof and measurement of association between two things, The American Journal of Psychology, 15, 72–101.
69. Stiratelli, Laird and Ware, 1984. Random-effects models for serial observations with binary response. Biometrics, 40, 961–971.
70. van Nierop W, Dusé AG, Marais E, Aithma N, Thothobolo N, Kassel M, Stewart R, Potgieter A, Fernandes B, Galpin JS and Bloomfield SF, 2005. Contamination of chicken carcasses in Gauteng, South Africa, by Salmonella, Listeria monocytogenes and Campylobacter, International Journal of Food Microbiology, 99, 1–6.
71. Wedderkopp A, Rattenborg E, Madsen M, 2000. National surveillance of Campylobacter in broilers at slaughter in Denmark in 1998, Avian Diseases, 44, 993–999.
72. Woldemariam E, Bouma A, Vernooij JC and Stegeman A, 2008. The sensitivity and specificity of fecal and cecal culture for the detection of Campylobacter in Dutch broiler flocks quantified by Bayesian analysis, International Journal of Food Microbiology, 121, 308–312.