Number of Salmonella on chicken breast filet at retail level and its implications for public health risk

Journal of Food Protection

Volumn 70, Issue 9, 2007, Pages 2045-2055

  Straver, J M ^a   Janssen, A F W ^a   Linnemann, A R ^a   Van Boekel, M A J S ^a   Beumer, R R ^a   Zwietering, M H ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COLUMBA; LACTUCA; SALMONELLA;

EID: 34748886357     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-70.9.2045     Document Type: Article

References (59)

1. Allen, V. M., J. E. L. Corry, C. H. Burton, R. T. Whyte, and G. C. Mead. 2000. Hygiene aspects of modern poultry chilling. Int. J. Food Microbiol. 58:39-48.
2. Canadian Food Inspection Agency. 2000. Canadian microbiological baseline study of chicken broiler and young turkey carcasses (June 1997-May 1998). Available at: http://www.inspection.gc.ca/english/anima/meavia/mmopmmhv/chap19/ baseline-e.pdf. Accessed 12 October 2006.
3. Cassin, M. H., A. M. Lammerding, E. C. D. Todd, W. Ross, and R. S. McColl. 1998. Quantitative risk assessment for Escherichia coli O157:H7 in ground beef hamburgers. Int. J. Food Microbiol. 41:21-44.
4. Cassin, M. H., G. M. Paoli, and A. M. Lammerding. 1998. Simulation modeling for microbial risk assessment. J. Food Prot. 61:1560-1566.
5. Chen, Y. H., K. M. Jackson, F. P. Chea, and D. W. Schaffner. 2001. Quantification and variability analysis of bacterial cross-contamination rates in common food service tasks. J. Food Prot. 64:72-80.
6. Chen, Y. H., E. H. Ross, V. N. Scott, and D. E. Gombas. 2003. Listeria monocytogenes: low levels equal low risk. J. Food Prot. 66:570-577.
7. Cooke, V. M., R. J. Miles, R. G. Price, and A. C. Richardson. 1999. A novel chromogenic ester agar medium for detection of salmonellae. Appl. Environ. Microbiol. 65:807-812.
8. de Man, J. C. 1983. MPN tables, corrected. Eur. J. Appl. Microbiol. 17:301-305.
9. Dufrenne, J., W. Ritmeester, E. Delfgou van Asch, F. van Leusden, and R. de Jonge. 2001. Quantification of the contamination of chicken and chicken products in The Netherlands with Salmonella and Campylobacter. J. Food Prot. 64:538-541.
10. Food and Agriculture Organization/World Health Organization. 2002. Risk assessments of Salmonella in eggs and broiler chickens. Available at: ftp://ftp.fao.org/docrep/faoy4392e/y4392e00.pdf. Accessed 12 October 2006.
11. Fravalo, P., Y. Hascoet, M. Le Fellic, S. Queguiner, J. Petton, and G. Salvat. 2003. Convenient method for rapid and quantitative assessment of Salmonella enterica contamination: the mini-MSRV MPN technique. J. Rapid Methods Autom. Microbiol. 11:81-88.
12. Gallagher, D. L., E. D. Ebel, and J. R. Kause. 2003. FSIS risk assessment for Listeria monocytogenes in deli meats. U.S. Department of Agriculture, Food Safety and Inspection Service, Washington, D.C. Available at: http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/97-013F/ListeriaReport.pdf. Accessed 12 October 2006.
13. Ghafir, Y., B. China, N. Korsak, K. Dierick, J. M. Collard, C. Godard, L. De Zutter, and G. Daube. 2005. Belgian surveillance plans to assess changes in Salmonella prevalence in meat at different production stages. J. Food Prot. 68:2269-2277.
14. Gorissen, L. Personal communication.
15. Hazeleger, W. C., J. A. Wouters, F. M. Rombouts, and T. Abee. 1998. Physiological activity of Campylobacter jejuni far below the minimal growth temperature. Appl. Environ. Microbiol. 64:3917-3922.
16. Heyndrickx, M., D. Vandekerchove, L. Herman, I. Rollier, K. Grijspeerdt, and L. de Zutter. 2002. Routes for Salmonella contamination of poultry meat: epidemiological study from hatchery to slaughter-house. Epidemiol. Infect. 129:253-265.
17. Holder, J. S., J. E. L. Corry, and M. H. Hinton. 1997. Microbial status of chicken portions and portioning equipment. Br. Poult. Sci. 38:505-511.
18. International Commission on Microbiological Specifications for Foods. 1996. Microorganisms in foods 5: microbiological specifications of food pathogens. Blackie Academic & Professional, New York.
19. Jorgensen, F., R. Bailey, S. Williams, P. Henderson, D. R. A. Wareing, F. J. Bolton, J. A. Frost, L. Ward, and T. J. Humphrey. 2002. Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. Int. J. Food Microbiol. 76:151-164.
20. Kasuga, F., M. Hirota, M. Wada, T. Yunokawa, H. Toyofuku, M. Shibatsuji, H. Michino, T. Kuwasaki, S. Yamamoto, and S. Kumagai. 2004. Archiving of food samples from restaurants and caterers - quantitative profiling of outbreaks of foodborne salmonellosis in Japan. J. Food Prot. 67:2024-2032.
21. Kemmeren, J. M., M. J. J. Mangen, Y. T. H. P. van Duynhoven, and A. H. Havelaar. 2006. Priority setting of foodborne pathogens - disease burden and costs of selected enteric pathogens. National Institute for Public Health and the Environment, Bilthoven, The Netherlands. Available at: http://www.rivm.nl/ bibliotheek/rapporten/330080001.pdf. Accessed 12 October 2006.
22. Kusumaningrum, H. D., G. Riboldi, W. C. Hazeleger, and R. R. Beumer. 2003. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. Int. J. Food Microbiol. 85:227-236.
23. Kusumaningrum, H. D., E. D. van Asselt, R. R. Beumer, and M. H. Zwietering. 2004. A quantitative analysis of cross-contamination of Salmonella and Campylobacter via the domestic kitchen surface. J. Food Prot. 67:1892-1903.
24. Laguerre, O., E. Derens, and B. Palagos. 2002. Study of domestic refrigerator temperatures and analysis of factors affecting temperature: a French study. Int. J. Refrig. 25:653-659.
25. Lammerding, A. M., and A. Fazil. 2000. Hazard identification and exposure assessment for microbial food safety risk assessment. Int. J. Food Microbiol. 58:147-157.
26. Legan, J. D., M. H. Vandeven, S. Dahms, and M. B. Cole. 2001. Determining the concentration of microorganisms controlled by attributes sampling plans. Food Control 12:137-147.
27. Lillard, H. S. 1990. The impact of commercial processing procedures on the bacterial contamination and cross-contamination of broiler carcasses. J. Food Prot. 53:202-204, 207.
28. Manafi, M. 2000. New developments in chromogenic and fluorogenic culture media. Int. J. Food Microbiol. 60(Special Issue):205-218.
29. Meldrum, R. J., R. M. M. Smith, and I. G. Wilson. 2006. Three-year surveillance program examining the prevalence of Campylobacter and Salmonella in whole retail chicken. J. Food Prot. 69:928-931.
30. Murphy, R. Y., B. P. Marks, E. R. Johnson, and M. G. Johnson. 1999. Inactivation of Salmonella and Listeria in ground chicken breast meat during thermal processing. J. Food Prot. 62:980-985.
31. Nauta, M. J., W. Jacobs-Reitsma, E. G. Evers, W. van Pelt, and A. H. Havelaar. 2005. Risk assessment of Campylobacter in The Netherlands via broiler meat and other routes. National Institute for Public Health and the Environment, Bilthoven, The Netherlands. Available at: http://www.rivm.nl/ bibliotheek/rapporten/250911006.pdf. Accessed 12 October 2006.
32. Nauta, M. J., W. F. Jacobs-Reitsma, and A. H. Havelaar. 2006. A risk assessment model for Campylobacter in broiler meat. Risk Anal. DOI: 10.1111/j.1539-6924.2006.00834.x.
33. Nauta, M. J., S. Litman, G. C. Barker, and F. Carlin. 2003. A retail and consumer phase model for exposure assessment of Bacillus cereus. Int. J. Food Microbiol. 83:205-218.
34. Oscar, T. P. 2006. Validation of a tertiary model for predicting variation of Salmonella Typhimurium DT104 (ATCC 700408) growth from a low initial density on ground chicken breast meat with a competitive microflora. J. Food Prot. 69:2048-2057.
35. Pérez-Rodríguez, F., E. D. van Asselt, R. M. García-Gimeno, G. Zurera, and M. H. Zwietering. 2007. Extracting additional risk managers information from a risk assessment of Listeria monocytogenes in deli meats. J. Food Prot. 70:1137-1152.
36. Perry, J. D., M. Ford, J. Taylor, A. L. Jones, R. Freeman, and F. K. Gould. 1999. ABC medium, a new chromogenic agar for selective isolation of Salmonella spp. J. Clin. Microbiol. 37:766-768.
37. Persson, E., I. Sjoholm, and K. Skog. 2002. Heat and mass transfer in chicken breasts - effect on PhIP formation. Eur. Food Res. Technol. 214:455-459.
38. Rall, V. L. M., R. Rail, L. C. Aragon, and M. G. da Silva. 2005. Evaluation of three enrichment broths and five plating media for Salmonella detection in poultry. Braz. J. Microbiol. 36:147-150.
39. Rasschaert, G., K. Houf, and L. De Zutter. 2006. Impact of the slaughter line contamination on the presence of Salmonella on broiler carcasses. J. Appl. Microbiol. DOI: 10.1111/j.1365-2672.2006.03248.x.
40. Restaino, L., K. K. Komatsu, and M. J. Syracuse. 1982. A note on novobiocin in XLD and HE agars: the optimum levels required in two commercial sources of media to improve isolation of salmonellas. J. Appl. Bacteriol. 53:285-288.
41. Rose, J. B., and C. P. Gerba. 1991. Use of risk assessment for development of microbial standards. Water Sci. Technol. 24:29-34.
42. Rosso, L., J. R. Lobry, S. Bajard, and J. P. Flandrois. 1995. Convenient model to describe the combined effects of temperature and pH on microbial growth. Appl. Environ. Microbiol. 61:610-616.
43. Sarlin, L. L., E. T. Barnhart, D. J. Caldwell, R. W. Moore, J. A. Byrd, D. Y. Caldwell, D. E. Corrier, J. R. Deloach, and B. M. Hargis. 1998. Evaluation of alternative sampling methods for Salmonella critical control point determination at broiler processing. Poult. Sci. 77:1253-1257.
44. Schalch, B., H. Eisgruber, and A. Stolle. 1996. Examination of minced meat for Salmonella using the modified semisolid-Rappaport-Vassiliadis medium (MSRV). Arch. Lebensmittelhyg. 47:112-114. (Abstract.)
45. Simmons, M., D. L. Fletcher, M. E. Berrang, and J. A. Cason. 2003. Comparison of sampling methods for the detection of Salmonella on whole broiler carcasses purchased from retail outlets. J. Food Prot. 66:1768-1770.
46. Stellbrink, E., and S. Dahms. 2004. Dose-response models and their implications for quantitative risk assessment for Campylobacter infections. Berl. Muench. Tieraerztl. Wochenschr. 117:207-213.
47. Tokumaru, M., H. Konuma, M. Umesako, S. Konno, and K. Shinagawa. 1991. Rates of detection of Salmonella and Campylobacter in meats in response to the sample size and the infection level of each species. Int. J. Food Microbiol. 13:41-46.
48. U.S. Department of Agriculture, Food Safety and Inspection Service. 1996. Nationwide broiler chicken microbiological baseline data collection program July 1994-June 1995. U.S. Department of Agriculture, Food Safety and Inspection Service, Washington, D.C. Available at: http://www.fsis.usda.gov/Ophs/baseline/ broiler1.pdf. Accessed 12 October 2006.
49. Uyttendaele, M., K. Baert, Y. Ghafir, G. Daube, L. de Zutter, L. Herman, K. Dierick, D. Pierard, J. J. Dubois, B. Horion, and J. Debevere. 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. Int. J. Food Microbiol. 111:149-163.
50. Uyttendaele, M. R., J. M. Debevere, R. M. Lips, and K. D. Neyts. 1998. Prevalence of Salmonella in poultry carcasses and their products in Belgium. Int. J. Food Microbiol. 40:1-8.
51. van der Zee, H., and B. Wit. 2005. Monitoring of pathogens on chicken and chicken products, year 2004. (In Dutch.) Dutch Food and Consumer Product Safety Authority, Zutphen, The Netherlands. Available at: http://www2.vwa.nl/CDL/ files/15/1004/10982%2020050915_Rapport_pathogenen_kip_2004.pdf. Accessed 12 October 2006.
52. van der Zee, H., B. Wit, and E. de Boer. 2001. Monitoring of pathogens on chicken and chicken products, year 2000. (In Dutch.) Dutch Food and Consumer Product Safety Authority, Zutphen, The Netherlands. Available at: http://www2.vwa.nl/CDL/files/15/1004/10401%202000_salmonella_campylobacter_kip. pdf. Accessed 12 October 2006.
53. van Gerwen, S. J. C., and M. H. Zwietering. 1998. Growth and inactivation models to be used in quantitative risk assessments. J. Food Prot. 61:1541-1549.
54. Vose, D. 2000. Risk analysis. John Wiley & Sons, Ltd., West Sussex, UK.
55. VWA (Food and Consumer Product Safety Authority). 2005. Zoonoses and zoonotic agents in humans, food, animals and feed in The Netherlands 2002. Dutch Food and Consumer Product Safety Authority. Available at: http://www2.vwa.nl/ CDL/files/15/1004/10503%2020041217_zoonoses_2002.pdf. Accessed 12 October 2006.
56. Whiting, R. C., and R. L. Buchanan. 1997. Development of a quantitative risk assessment model for Salmonella enteritidis in pasteurized liquid eggs. Int. J. Food Microbiol. 36:111-125.
57. Wilson, I. G. 2002. Salmonella and Campylobacter contamination of raw retail chickens from different producers: a six year survey. Epidemiol. Infect. 129:635-645.
58. Zhao, C. W., B. L. Ge, J. De Villena, R. Sudler, E. Yeh, S. H. Zhao, D. G. White, D. Wagner, and J. H. Meng. 2001. Prevalence of Campylobacter spp., Escherichia coli, and Salmonella serovars in retail chicken, turkey, pork, and beef from the Greater Washington, DC, area. Appl. Environ. Microbiol. 67:5431-5436.
59. Zhao, P., T. Zhao, M. P. Doyle, J. R. Rubino, and J. Meng. 1998. Development of a model for evaluation of microbial cross-contamination in the kitchen. J. Food Prot. 61:960-963.