Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens

International Journal of Food Microbiology

Volumn 83, Issue 1, 2003, Pages 87-103

  Rosenquist, Hanne ^a   Nielsen, Niels L ^a   Sommer, Helle M ^a   Nørrung, Birgit ^a   Christensen, Bjarke B ^a  

^a DANISH VETERINARY AND FOOD ADMINISTRATION   (Denmark)

Author keywords

Campylobacter; Campylobacter jejuni; Chickens; Mitigations; Monte Carlo simulation; Quantitative risk assessment; Risk

Indexed keywords

ARTICLE; BACTERIAL INFECTION; BACTERIAL TRANSMISSION; BACTERIUM CONTAMINATION; CAMPYLOBACTER; CARCASS; CHICKEN; CONSUMER; DENMARK; FOOD CONTAMINATION; FOOD HANDLING; FOOD INTAKE; FOOD PROCESSING; FOOD SAFETY; HIGH RISK POPULATION; HYGIENE; MATHEMATICAL MODEL; MEAL; MEAT; QUANTITATIVE ANALYSIS; RISK ASSESSMENT; SIMULATION; SLAUGHTERHOUSE; THERMOPHILIC BACTERIUM;

ABATTOIRS; ADOLESCENT; ADULT; AGED; ANIMAL HUSBANDRY; ANIMALS; CAMPYLOBACTER; CAMPYLOBACTER INFECTIONS; CHICKENS; DENMARK; DISEASE OUTBREAKS; FEMALE; FOOD CONTAMINATION; FOOD HANDLING; FOOD MICROBIOLOGY; FOOD-PROCESSING INDUSTRY; HUMANS; HYGIENE; MALE; MIDDLE AGED; MONTE CARLO METHOD; RISK ASSESSMENT;

CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; GALLUS GALLUS;

EID: 0037466725     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-1605(02)00317-3     Document Type: Article

References (78)

1. Adak G.K., Cowden J.M., Nicholas S., Evans H.S. The public health laboratory service national case-control study of primary indigenous sporadic cases of Campylobacter infection. Epidemiol. Infect. 115:1995;15-22.
2. AIM Nielsen og Levnedsmiddelstyrelsen, 1997. Hygiejne-Temperaturmåling i køleskabe (In Danish).
3. Allos B.M. Association between Campylobacter infection and Guillain-Barré syndrome. J. Infect. Dis. 176:1997;S125-S128.
4. Allos B.M., Blaser M.J. Campylobacter jejuni and the expanding spectrum of related infections. Clin. Infect. Dis. 20:1995;1092-1101.
5. Altekruse S.F., Street D.A., Fein S.B., Levy A.S. Consumer knowledge of food-borne microbial hazards and food-handling practices. J. Food Prot. 59:1995;287-294.
6. Andersen N.L., Fagt S., Groth M.V., Hartkopp H.B., Møller A., Ovesen L., Warming D.L. Dietary habits in Denmark, 1995 (in Danish). The National Food Agency. Publication no. 235:1996.
7. Anonymous Annual Report on Zoonosis in Denmark 1994. 1995;Minestry of Food, Agriculture and Fisheries, Denmark.
8. Anonymous Annual Report on Zoonosis in Denmark 1995. 1996;Minestry of Food, Agriculture and Fisheries, Denmark.
9. Anonymous Annual Report on Zoonosis in Denmark 1996. 1997;Minestry of Food, Agriculture and Fisheries, Denmark.
10. Anonymous Annual Report on Zoonosis in Denmark 1997. 1998;Minestry of Food, Agriculture and Fisheries, Denmark.
11. Anonymous Annual Report on Zoonosis in Denmark 1998. 1999;Minestry of Food, Agriculture and Fisheries, Denmark.
12. Anonymous Guidelines Regarding Pathogenic Micro-organisms in Foods. 1999;The Danish Veterinary and Food Administration, Sobory, Denmark.
13. Anonymous, 1999c. Trends and sources of zoonotic agents in animals, feedstuffs, food and man in the European Union in 1997. Part 1. Document No. VI/8495/98-Rev. 2 of the European Commission, Community Reference Laboratory on the Epidemiology of Zoonoses, BgVV, Berlin, Germany.
14. Anonymous Annual Report on Zoonosis in Denmark 1999. 2000;Minestry of Food, Agriculture and Fisheries, Denmark.
15. Anonymous Annual Report on Zoonoses in Denmark 2000. 2001;Minestry of Food Agriculture and Fisheries, Denmark.
16. Anonymous, 2001b. Trends and sources of zoonotic agents in animals, feeding stuff, food and man in the European Union and Norway in 1999. Part 1. Document No. SANCO/1069/2001 of the European Commission, Community Reference Laboratory on the Epidemiology of Zoonoses, BgVV, Berlin, Germany.
17. Berndtson, E., 1996. Campylobacter in broiler chickens. The mode of spread in chicken flocks with special reference to food hygiene. PhD Thesis, Swedish University of Agricultural Sciences, Department of Food Hygiene. SLU Repro, Uppsala.
18. Berndtson E., Danielsson-Tham M.L., Engvall A. Campylobacter incidence on a chicken farm and the spread of Campylobacter during the slaughter process. Int. J. Food Microbiol. 32:1996;35-47.
19. Black R.E., Levine M.M., Clements M.L., Hughes T.P., Blaser M. Experimental Campylobacter jejuni infection in humans. J. Infect. Dis. 157:1988;472-479.
20. Blankenship L.C., Craven S.E. Campylobacter jejuni survival in chicken meat as a function of temperature. Appl. Environ. Microbiol. 44:1982;88-92.
21. Blaser M.J., Taylor D.N., Feldman R.A. Epidemiology of Campylobacter jejuni infections. Epidemiol. Rev. 5:1983;157-176.
22. Codex Alimentarius Commission (CAC), 1999. Principles and Guidelines for the Conduct of Microbiological Risk Assessment. Joint FAO/WHO food standards programme. Codex Committee on Food Hygiene, 32th session, Rome, Italy, 28, June-3 July 1999.
23. Center for Alternativ Samfundsanalyse (CASA), 1999. Køkkenhygiejne i danske husstande-viden og adfærd (In Danish).
24. Chen Y., Jackson K.M., Chea F.P., Schaffner D.W. Quantification and variability analysis of bacterial cross-contamination rates in common food service tasks. J. Food Prot. 62:2001;72-80.
25. Coleman M., Marks H. Topics in dose-response modelling. J. Food Prot. 61:1998;1550-1559.
26. Daniels R.W. Home food safety. Food Technol. 52:1998;54-56.
27. Deming M.S., Tauxe R.V., Blake P.A., Blake S.E., Dixon S.E., Fowler B.S., Jones T.S., Lockamy E.A., Patton C.M., Sikes R.O. Campylobacter enteritis at a university from eating chickens and from cats. Am. J. Epidemiol. 126:1987;526-534.
28. Effler P., Ieong M.-C., Kimura A., Nakata M., Burr R., Cremer E., Slutsker L. Sporadic Campylobacter infections in Hawaii: associations with Prior antibiotic use and commercially prepared chicken. J. Infect. Dis. 183:2001;1152-1155.
29. FAO/WHO, 1995. Application of Risk Analysis to Food Standard Issues. Report of the Joint FAO/WHO Expert Consultation. Geneva, Switzerland, 13-17 March 1995. WHO: Geneva.
30. FAO/WHO, 1997. Risk Management and Food Safety. Report of a Joint FAO/WHO Consultation. Rome, Italy, 27-31 January 1997. Rome: FAO.
31. Friedman C.R., Neimann J., Wegener H.C., Tauxe R.V. Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. Nachamkin I., Blaser M.J. Campylobacter. 2000;121-138 American Society for Microbiology, Washington, DC.
32. Friedman C., Reddy S., Samuel M., Marcus R., Bender J., Desai S., Shiferaw B., Helfrick D., Carter M., Anderson B., Hoekstra M. Risk factors for sporadic Campylobacter infections in the United States: a case-control study on FoodNet sites. 2nd International Conference on Emerging Infectious Diseases. Atlanta, GA, July 2000:2000;. (http://www.cdc.gov/foodnet/pub/iceid/2000/friedman_c.htm).
33. Griffith C., Worsfold D., Mitchell R. Food preparation, risk communication and the consumer. Food Control. 9:1998;225-232.
34. Haas C.N. Estimation of risk due to low doses of microorganisms: a comparison of alternative methodologies. Am. J. Epidemiol. 118:1983;573-582.
35. Hänninen M.-K. Survival of Campylobacter jejuni/coli in ground refrigerated and in ground frozen beef liver and in frozen broiler carcasses. Acta Vet. Scand. 22:1981;566-577.
36. Harris N.V., Weiss N.S., Nolan C.M. The role of poultry and meats in the etiology of Campylobacter jejuni/coli enteritis. Am. J. Public Health. 76:1986;407-411.
37. Hopkins R.S., Olmsted R., Istre G.R. Endemic Campylobacter jejuni infection in Colorado: identified risk factors. Am. J. Public Health. 74:1984;249-250.
38. Humphrey T.J., Lanning D.G. Salmonella and Campylobacter contamination of broiler chicken carcasses and scald tank water: the influence of water pH. J. Appl. Bacteriol. 63:1987;21-25.
39. Humphrey T.J., Henley A., Lanning D.G. The colonization of broiler chickens with Campylobacter jejuni: some epidemiological investigations. Epidemiol. Infect. 110:1993;601-607.
40. Microorganisms in foods 5. Characteristics of Microbial Pathogens. 1996;45-65 Blackie Academic and Professional, London.
41. Principles for the establishment of microbiological food safety objectives and related control measures. Food Control. 9:1998;379-384.
42. Ikram R. A case control study to determine risk factors for Campylobacter infection in Christchurch in the summer of 1992-3. N. Z. Med. J. 107:1994;430-432.
43. Izat A.L., Gardner F.A., Denton J.H., Golan F.A. Incidence and level of Campylobacter jejuni in broiler processing. Poult. Sci. 67:1988;1568-1572.
44. Jay L.S., Comar D., Govenlock L.D. A national Australian food safety telephone survey. J. Food Prot. 62:1999;921-928.
45. Kapperud G. Campylobacter infections. Epidemiology, risk factors and preventive measures (in Norwegian). Tidsskr. Nor. Laegeforen. 114:1994;795-799.
46. Kapperud G., Skjerve E., Bean N.H., Ostroff S.M., Lassen J. Risk factors for sporadic Campylobacter infections: results of a case-control study in Southeastern Norway. J. Clin. Microbiol. 30:1992;3117-3121.
47. Kapperud G., Skjerve E., Vik L., Hauge K., Lysaker A., Aalmen I., Ostroff S.M., Potter M. Epidemiological investigations of risk factors for Campylobacter colonization in Norwegian broiler flocks. Epidemiol. Infect. 111:1993;245-255.
48. Mead G.C., Hudson W.R., Hinton M.H. Effect of changes in processing to improve hygiene control on contamination of poultry carcasses with Campylobacter. Epidemiol. Infect. 115:1995;495-500.
49. Medema G.J., Teunis P.F.M., Havelaar A.H., Haas C.N. Asessment of the dose-response relationship of Campylobacter jejuni. Int. J. Food Microbiol. 30:1996;101-111.
50. Mishu B., Blaser M.J. Role of infection due to Campylobacter jejuni in the initiation of Guillain-Barré Syndrome. Clin. Infect. Dis. 17:1993;104-108.
51. Mishu B., Ilyas A.A., Koski C.L., Vriesendorp F., Cook S.D., Mithen F.A., Blaser M.J. Serologic evidence of previous Campylobacter jejuni infection in patients with the Guillain-Barré Syndrome. Ann. Intern. Med. 118:1993;947-953.
52. Neal K.R., Slack R.C. The autumn peak in Campylobacter gastro enteritis. Are the risk factors the same for travel- and UK-acquired Campylobacter infections? J. Public Health Med. 17:1995;98-102.
53. Neimann, J., 2001. The epidemiology of sporadic campylobacteriosis in Denmark investigated by a case control study and strain characterization of patient isolates. PhD thesis. Danish Zoonosis Center, Danish Veterinary Laboratory. Vester Kopi, Valby.
54. Norkrans G., Svedheim A. Epidemiological aspects of Campylobacter jejuni enteritis. J. Hyg. (Lond.). 89:1982;163-170.
55. Oosterom J., Notermans S., Karman H., Engels G.B. Origin and prevalence of Campylobacter jejuni in poultry processing. J. Food Prot. 46:1983;339-344.
56. Oosterom J., de Wilde G.J.A., de Boer E., de Blaauw L.H., Karman H. Survival of Campylobacter jejuni during poultry processing and pig slaughtering. J. Food Prot. 46:1983;702-706.
57. Oosterom J., den Uyl C.H., Bänffer J.R.J., Huisman J. Epidemiological investigations on Campylobacter jejuni in households with primary infection. J. Hyg. (Lond.). 92:1984;325-332.
58. Othsuka K., Nakamura Y., Hashimoto M., Tagawa Y., Takahashi M., Saito K., Yuki N. Fisher syndrome associated with IgG anti GQ1b antibody following infection by a specific serotype of Campylobacter jejuni. Ophthalmology. 105:1988;1281-1285.
59. Peterson M.C. Rheumatic manifestations of Campylobacter jejuni and C. fetus infections in adults. Scand. J. Rheumatol. 23:1994;167-170.
60. Piddock L.J.V. Quinolone resistance and Campylobacter spp. Antimicrob. Chemother. 36:1995;891-898.
61. Piddock L.J.V. Implications for human health. Antimicrob. Chemother. Suppl. A. 44:1999;17.
62. Reiersen J., Briem H., Hardardottir H., Gunnarsson E., Georgsson F., Kristinsson K.G. Human campylobacteriosis epidemic in Iceland 1998-2000 and effect of interventions aimed at poultry and humans. Int. J. Med. Microbiol. 291(Suppl. 31):2001;153.
63. Robinson D.A. Infective dose of Campylobacter jejuni in milk. BMJ. 282:1981;1584.
64. Rosenfield J.A., Arnold G.J., Davey G.R., Archer R.S., Woods W.H. Serotyping of Campylobacter jejuni from an outbreak of enteritis implicating chicken. J. Infect. 11:1985;159-165.
65. Saeed A.M., Harris N.V., DiGiacomo R.F. The role of exposure to animals in the etiology of Campylobacter jejuni/coli enteritis. Am. J. Epidemiol. 137:1993;108-114.
66. Schorr D., Schmid H., Rieder H.L., Baumgartner A., Vorkauf H., Burnens A. Risk factors for Campylobacter enteritis in Switzerland. Zbl. Hyg. 196:1994;327-337.
67. Skirrow M.B. Epidemiology of Campylobacter enteritis. Int. J. Food Microbiol. 12:1991;9-16.
68. Stern N.J. Mucosal competitive exclusion to diminish colonization of chickens by Campylobacter jejuni. Poult. Sci. 73:1994;402-407.
69. Vose D.J. Quantitative Risk Analysis: A Guide to Monte Carlo Simulation Modelling. 2000;Wiley, Chichester.
70. Wheeler J.G., Sethi D., Cowden J.M., Wall P.G., Rodrigues L.C., Tompkins D.S., Hudson M.J., Roderick P.J. Study of infectious intestinal disease in England: rates in the community, presenting to general practice, and reported to national surveillance. BMJ. 318:1999;1046-1050.
71. WHO, 2001. The increasing incidence of human campylobacteriosis. Report and proceedings of a WHO consultation of experts, Copenhagen, Denmark, 21-25 November 2000.
72. Widders P.R., Perry R., Muir W.I., Husband A.J., Long K.A. Immunisation of chickens to reduce intestinal colonisation with Campylobacter jejuni. Br. Poult. Sci. 37:1996;765-778.
73. Williamson D.M., Gravani R.B., Lawless H. Correlating food safety knowledge with home food-preparation practices. Food Technol. 46:1992;94-100.
74. Worsfold D., Griffith C.J. Assessment of the standard consumer food safety behavior. J. Food Prot. 60:1997;399-406.
75. WTO, 1994. Agreement on the Application of Sanitary and Phytosanitary Measures. The Final Act of the 1986-1994 Uruguay Round of Trade Negotiations.
76. Yang S., Leff M.G., Mctague D., Horvath K.A., Jackson-Thompson J., Murayi T., Boeselager G.K., Melnik T.A., Gildemaster M.C., Ridings D.L., Altekruse S.F., Angulo F.J. Multistate surveillance for food-handling, preparation, and consumption behaviors associated with food-borne diseases: 1995 and 1996 BRFSS Food-Safety Questions. Mor. Mortal. Wkly. Rep. CDC Surveill. Summ. September 11. vol. 47(SS-4):1998;33-54.
77. Yogasundram K., Shane S.M. The viability of Campylobacter jejuni on refrigerated chicken drumsticks. Vet. Res. Commun. 10:1986;479-486.
78. Zhao P., Zhao T., Doyle M.P., Rubino J.R., Meng J. Development of a model for evaluation of microbial cross-contamination in the kitchen. J. Food Prot. 61:1998;960-963.