Microbiological baseline study of swine carcasses at Swedish slaughterhouses

Journal of Food Protection

Volumn 70, Issue 8, 2007, Pages 1790-1797

  Lindblad, M ^a   Lindmark, H ^a   Thisted Lambertz, S ^a   Lindqvist, R ^a  

^a NATIONAL FOOD ADMINISTRATION   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); CAMPYLOBACTER; ENTEROBACTERIACEAE; ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; SALMONELLA; STAPHYLOCOCCUS; SUIDAE; YERSINIA ENTEROCOLITICA;

EID: 34547753414     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-70.8.1790     Document Type: Article

References (76)

1. Adesiyun, A. A., and C. Krishnan. 1995. Occurrence of Yersinia enterocolitica O:3, Listeria monocytogenes O:4 and thermophilic Campylobacter spp. in slaughter pigs and carcasses in Trinidad. Food Microbiol. 12:99-107.
2. Alter, T., F. Gaull, S. Kasimir, M. Gurtler, and K. Fehlhaber. 2005. Distribution and genetic characterization of porcine Campylobacter coli isolates. Berl. Muench. Tierarztl. Wochenschr. 118:214-219.
3. Anonymous. 1997. Risk management and food safety. Report of a Joint FAO/WHO Consultation, Rome, 27 to 31 January 1997.
4. Anonymous. 2001. Commision decision of 8 June 2001. Off. J. Eur. Union L 165:48-53.
5. Anonymous. 2004. Trends and sources of zoonotic agents in animals, feedingstuffs, food and man in the European Union and Norway in 2003. Available at: http://ec.europa.eu/food/food/biosafety/salmonella/zoonoses_reps_en.htm. Accessed 27 December 2006.
6. Anonymous. 2005. Commision regulation (EC) 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Off. J. Eur. Union L 338:1-25.
7. Autio, T., T. Sateri, M. Fredriksson Ahomaa, M. Rahkio, J. Lunden, and H. Korkeala. 2000. Listeria monocytogenes contamination pattern in pig slaughterhouses. J. Food Prot. 63:1438-1442.
8. Berends, B. R., F. Van Knapen, D. A. Mossel, S. A. Burt, and J. M. Snijders. 1998. Impact on human health of Salmonella spp. on pork in The Netherlands and the anticipated effects of some currently proposed control strategies. Int. J. Food Microbiol. 44:219-229.
9. Beutin, L., D. Geier, H. Steinruck, S. Zimmermann, and F. Scheutz. 1993. Prevalence and some properties of verotoxin (Shiga-like toxin)-producing Escherichia coli in seven different species of healthy domestic animals. J. Clin. Microbiol. 31:2483-2488.
10. Bhaduri, S., I. V. Wesley, and E. J. Bush. 2005. Prevalence of pathogenic Yersinia enterocolitica strains in pigs in the United States. Appl. Environ. Microbiol. 71:7117-7121.
11. Biedzka-Sarek, M., R. Venho, and M. Skurnik. 2005. Role of yadA, ail, and lipopolysaccharide in serum resistance of Yersinia enterocolitica serotype O:3. Infect. Immun. 73:2232-2244.
12. Boes, J., L. Nersting, E. M. Nielsen, S. Kranker, C. Enoe, H. C. Wachmann, and D. L. Baggesen. 2005. Prevalence and diversity of Campylobacter jejuni in pig herds on farms with and without cattle or poultry. J. Food Prot. 68:722-727.
13. Bonardi, S., F. Brindani, G. Pizzin, L. Lucidi, M. D'Incau, E. Liebana, and S. Morabito. 2003. Detection of Salmonella spp., Yersinia enterocolitica and verocytotoxin-producing Escherichia coli O157 in pigs at slaughter in Italy. Int. J. Food Microbiol. 85:101-110.
14. Borch, E., T. Nesbakken, and H. Christensen. 1996. Hazard identification in swine slaughter with respect to foodborne bacteria. Int. J. Food Microbiol. 30:9-25.
15. Botteldoorn, N., M. Heyndrickx, N. Rijpens, and L. Herman. 2003. Detection and characterization of verotoxigenic Escherichia coli by a VTEC/EHEC multiplex PCR in porcine faeces and pig carcass swabs. Res. Microbiol. 154:97-104.
16. Bouvet, J., M. P. Montet, R. Rossel, A. Roux, C. Bavai, S. Ray-Gueniot, C. Mazuy, V. Attache, and C. Vernozy-Rozand. 2002. Prevalence of verotoxin-producing Escherichia coli (VTEC) and E. coli O157:H7 in French pork. J. Appl. Microbiol. 93:7-14.
17. Boyapalle, S., I. V. Wesley, H. S. Hurd, and P. G. Reddy. 2001. Comparison of culture, multiplex, and 5′ nuclease polymerase chain reaction assays for the rapid detection of Yersinia enterocolitica in swine and pork products. J. Food Prot. 64:1352-1361.
18. Buchanan, R. L., and R. C. Whiting. 1998. Risk assessment: a means for linking HACCP plans and public health. J. Food Prot. 61:1531-1534.
19. Casman, E. P., D. W. McCoy, and P. J. Brandly. 1963. Staphylococcal growth and enterotoxin production in meat. Appl. Microbiol. 11:498-500.
20. Chang, V. P., E. W. Mills, and C. N. Cutter. 2003. Reduction of bacteria on pork carcasses associated with chilling method. J. Food Prot. 66:1019-1024.
21. Duffy, E. A., K. E. Belk, J. N. Sofos, G. R. Bellinger, A. Pape, and G. C. Smith. 2001. Extent of microbial contamination in United States pork retail products. J. Food Prot. 64:172-178.
22. Eblen, D. R., P. Levine, B. E. Rose, P. Saini, R. Mageau, and W. E. Hill. 2005. Nationwide microbiological baseline data collected by sponge sampling during 1997 and 1998 for cattle, swine, turkeys, and geese. J. Food Prot. 68:1848-1852.
23. Epling, L. K., J. A. Carpenter, and L. C. Blankenship. 1993. Prevalence of Campylobacter spp. and Salmonella spp. on pork carcasses and the reduction effected by spraying with lactic acid. J. Food Prot. 56:536-537.
24. Fermer, C., and E. O. Engvall. 1999. Specific PCR identification and differentiation of the thermophilic campylobacters, Campylobacter jejuni, C. coli, C. lari, and C. upsaliensis. J. Clin. Microbiol. 37:3370-3373.
25. Fredriksson-Ahomaa, M., J. Bjorkroth, S. Hielm, and H. Korkeala. 2000. Prevalence and characterization of pathogenic Yersinia enterocolitica in pig tonsils from different slaughterhouses. Food Microbiol. 17:93-101.
26. Fredriksson-Ahomaa, M., S. Hielm, and H. Korkeala. 1999. High prevalence of yadA-positive Yersinia enterocolitica in pig tongues and minced meat at the retail level in Finland. J. Food Prot. 62:123-127.
27. Fredriksson-Ahomaa, M., T. Korte, and H. Korkeala. 2000. Contamination of carcasses, offals, and the environment with yadA-positive Yersinia enterocolitica in a pig slaughterhouse. J. Food Prot. 63:31-35.
28. Fredriksson-Ahomaa, M., A. Stolle, A. Siitonen, and H. Korkeala. 2006. Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O:3 originate mainly from pigs. J. Med. Microbiol. 55:747-749.
29. Funk, J. A., H. F. Troutt, R. E. Isaacson, and C. P. Fossler. 1998. Prevalence of pathogenic Yersinia enterocolitica in groups of swine at slaughter. J. Food Prot. 61:677-682.
30. Gannon, V. P., S. D'Souza, T. Graham, R. K. King, K. Rahn, and S. Read. 1997. Use of the flagellar H7 gene as a target in multiplex PCR assays and improved specificity in identification of enterohemorrhagic Escherichia coli strains. J. Clin. Microbiol. 35:656-662.
31. Gebreyes, W. A., S. Thakur, and W. E. Morrow. 2005. Campylobacter coli: prevalence and antimicrobial resistance in antimicrobial-free (ABF) swine production systems. J. Antimicrob. Chemother. 56:765-768.
32. Ghafir, Y., G. Daube, K. Dierick, L. De Zutter, M. Cornelis, and M. Jouret. 2003. Assessment of microbiological criteria for regular checks of faecal contamination and general hygiene in Belgian establishments producing meat. Sci. Aliment. 23:104-106.
33. Gill, C.-O., and T. Jones. 1997. Assessment of the hygienic characteristics of a process for dressing pasteurized pig carcasses. Food Microbiol. 14:81-91.
34. Gurtler, M., T. Alter, S. Kasimir, M. Linnebur, and K. Fehlhaber. 2005. Prevalence of Yersinia enterocolitica in fattening pigs. J. Food Prot. 68:850-854.
35. Hald, T., D. Vose, H. C. Wegener, and T. Koupeev. 2004. A Bayesian approach to quantify the contribution of animal-food sources to human salmonellosis. Risk Anal. 24:255-269.
36. Johannessen, G. S., G. Kapperud, and H. Kruse. 2000. Occurrence of pathogenic Yersinia enterocolitica in Norwegian pork products determined by a PCR method and a traditional culturing method. Int. J. Food Microbiol. 54:75-80.
37. Kanuganti, S. R., I. V. Wesley, P. G. Reddy, J. McKean, and H. S. Hurd. 2002. Detection of Listeria monocytogenes in pigs and pork. J. Food Prot. 65:1470-1474.
38. Kapperud, G. 1991. Yersinia enterocolitica in food hygiene. Int. J. Food Microbiol. 12:53-66.
39. Kilsby, D. C., and M. E. Pugh. 1981. The relevance of the distribution of micro-organisms within batches of food to the control of microbiological hazards from foods. J. Appl. Bacteriol. 51:345-354.
40. Korte, T., M. Fredriksson-Ahomaa, T. Niskanen, and H. Korkeala. 2004. Low prevalence of yadA-positive Yersinia enterocolitica in sows. Foodborne Pathog. Dis. 1:45-52.
41. LaGier, M. J., L. A. Joseph, T. V. Passaretti, K. A. Musser, and N. M. Cirino. 2004. A real-time multiplexed PCR assay for rapid detection and differentiation of Campylobacter jejuni and Campylobacter coli. Mol. Cell. Probes 18:275-282.
42. 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.
43. Letellier, A., S. Messier, and S. Quessy. 1999. Prevalence of Salmonella spp. and Yersinia enterocolitica in finishing swine at Canadian abattoirs. J. Food Prot. 62:22-25.
44. Lindblad, M., H. Lindmark, S. Thisted Lambertz, and R. Lindqvist. 2006. Microbiological baseline study of broiler chickens at Swedish slaughterhouses. J. Food Prot. 12:2875-2882.
45. Lindqvist, R. 1997. Preparation of PCR samples from food by a rapid and simple centrifugation technique evaluated by detection of Escherichia coli O157:H7. Int. J. Food Microbiol. 37:73-82.
46. Mafu, A. A., R. Higgins, M. Nadeau, and G. Cousineau. 1989. The incidence of Salmonella, Campylobacter, and Yersinia enterocolitica in swine carcasses and the slaughterhouse environment. J. Food Prot. 52:642-645.
47. Marques, L. R. M., J. S. M. Peiris, S. J. Cryz, and A. D. O'Brien. 1987. Escherichia coli strains isolated from pigs with edema disease produce a variant of Shiga-like toxin II. FEMS Microbiol. Lett. 44:33-38.
48. National Veterinary Institute. 2006. Zoonoses in Sweden 2005. Available at: http://www.sva.se. Accessed 27 December 2006.
49. Nesbakken, T., T. Iversen, K. Eckner, and B. Lium. 2006. Testing of pathogenic Yersinia enterocolitica in pig herds based on the natural dynamic of infection. Int. J. Food Microbiol. 111:99-104.
50. Nesbakken, T., G. Kapperud, and D. A. Caugant. 1996. Pathways of Listeria monocytogenes contamination in the meat processing industry. Int. J. Food Microbiol. 31:161-171.
51. Nesbakken, T., E. Nerbrink, O. J. Rotterud, and E. Borch. 1994. Reduction of Yersinia enterocolitica and Listeria spp. on pig carcasses by enclosure of the rectum during slaughter. Int. J. Food Microbiol. 23:197-208.
52. Nesbakken, T., and E. Skjerve. 1996. Interruption of microbial cycles in farm animals from farm to table. Meat Sci. 43:S47-S57.
53. Newcombe, R. G. 1998. Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat. Med. 17:857-872.
54. Nogva, H. K., A. Bergh, A. Holck, and K. Rudi. 2000. Application of the 5′-nuclease PCR assay in evaluation and development of methods for quantitative detection of Campylobacter jejuni. Appl. Environ. Microbiol. 66:4029-4036.
55. Nordic Committee on Food Analysis. 1990. Campylobacter jejuni/coli. Detection in foods. Method 119, 2nd ed. NMKL secretariat, Norway.
56. Nordic Committee on Food Analysis. 1999. Aerobic microorganisms. Determination in foods. Method 86, 3rd ed. NMKL secretariat, Norway.
57. Nordic Committee on Food Analysis. 1999. Salmonella. Detection in foods. Method 71, 5th ed. NMKL secretariat, Norway.
58. Nordic Committee on Food Analysis. 2000. Enterobacteriaceae. Determination in foods and feeds. Method 144, 2nd ed. NMKL secretariat, Norway.
59. Nordic Committee on Food Analysis. 2003. Staphylococcus aureus. Enumeration in foods. Method 66, 4th ed. NMKL secretariat, Norway.
60. Nordic Committee on Food Analysis. 2004. Listeria monocytogenes. Detection in foods and feeds. Method 136, 3rd ed. NMKL secretariat, Norway.
61. Nordic Committee on Food Analysis. 2005. Thermotolerant coliform bacteria and Escherichia coli. Enumeration in food and feed. Method 125, 4th ed. NMKL secretariat, Norway.
62. Oosterom, J., R. Dekker, G. J. A. de Wilde, F. van Kempen-de Troye, and G. B. Engels. 1985. Prevalence of Campylobacter jejuni and Salmonella during pig slaughtering. Vet. Q. 7:31-34.
63. Ostroff, S. M., G. Kapperud, L. C. Hutwagner, T. Nesbakken, N. H. Bean, J. Lassen, and R. V. Tauxe. 1994. Sources of sporadic Yersinia enterocolitica infections in Norway: a prospective case-control study. Epidemiol. Infect. 112:133-141.
64. Pass, M. A., R. Odedra, and R. M. Batt. 2000. Multiplex PCRs for identification of Escherichia coli virulence genes. J. Clin. Microbiol. 38:2001-2004.
65. O157. J. Clin. Microbiol. 36:598-602.
66. Pearce, R. A., F. M. Wallace, J. E. Call, R. L. Dudley, A. Oser, L. Yoder, J. J. Sheridan, and J. B. Luchansky. 2003. Prevalence of Campylobacter within a swine slaughter and processing facility. J. Food Prot. 66:1550-1556.
67. Saide Albornoz, J. J., C. L. Knipe, E. A. Murano, and G. W. Beran. 1995. Contamination of pork carcasses during slaughter, fabrication, and chilled storage. J. Food Prot. 58:993-997.
68. Schraft, H., N. Kleinlein, and F. Untermann. 1992. Contamination of pig hindquarters with Staphylococcus aureus. Int. J. Food Microbiol. 15:191-194.
69. Sørensen, R., and H. Christensen. 1997. Campylobacter i svinekødet problem? Dan. Veterinaertidsskr. 80:452-453. (In Danish.)
70. Swedish Institute for Infectious Disease Control. 2006. Surveillance statistics. Available at: http://www.smittskyddsinstitutet.se/statistik/ yersiniainfektion/?t=week. Accessed 27 December 2006.
71. Thévenot, D., A. Dernburg, and C. Vernozy-Rozand. 2006. An updated review of Listeria monocytogenes in the pork meat industry and its products. J. Appl. Microbiol. 101:7-17.
72. Thisted Lambertz, S. 2005. Development of a PCR-based method for detection of pathogenic Yersinia enterocolitica in pork. Ph.D. thesis. Swedish University of Agricultural Sciences, Uppsala.
73. Thisted Lambertz, S., R. Lindqvist, A. Ballagi-Pordany, and M.-L. Danielsson-Tham. 2000. A combined culture and PCR method for detection of pathogenic Yersinia enterocolitica in food. Int. J. Food Microbiol. 57:63-73.
74. U.S. Department of Agriculture, Food Safety and Inspection Service. 1996. Nationwide pork microbiological baseline data collection program: market hogs. Available at: http://www.fsis.usda.gov/Science/BaselinepData/index.asp. Accessed 27 December 2006.
75. Yeh, K. S., S. P. Chen, and J. H. Lin. 2005. One-year (2003) nationwide pork carcass microbiological baseline data survey in Taiwan. J. Food Prot. 68:458-461.
76. Zhao, C., B. Ge, J. De Villena, R. Sudler, E. Yeh, S. Zhao, D. G. White, D. Wagner, and J. Meng. 2001. Prevalence of Campylobacter spp., Escherichia coli, and Salmonella serovars in retail chicken, turkey, pork, and beef from the Greater Washington, D.C., area. Appl. Environ. Microbiol. 67:5431-5436.