Assessing interventions by quantitative risk assessment tools to reduce the risk of human salmonellosis from fresh minced pork meat in Belgium

Journal of Food Protection

Volumn 72, Issue 11, 2009, Pages 2252-2263

  Delhalle, L ^a   Saegerman, C ^a   Messens, W ^b   Farnir, F ^a   Korsak, N ^a   Van Der Stede, Y ^c   Daube, G ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b INSTITUTE FOR AGRICULTURAL AND FISHERIES RESEARCH ILVO   (Belgium)

^c VETERINARY AND AGROCHEMICAL RESEARCH CENTRE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 70449572258     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-72.11.2252     Document Type: Article

References (92)

1. Agence fédérale pour la sécurite de la chaine alimentaire (AFSCA). 2007. Activity report 2006, p. 186. Federal Food Agency, Brussels.
2. 2. Alban, L., and K. D. C. Stark. 2005. Where should the effort be put to reduce the Salmonella prevalence in the slaughtered swine carcass effectively? Prev. Vet. Med. 68:63-79. (Pubitemid 40413302)
3. Anonymous. 2006. Annual report on zoonoses in Denmark 2005, p. 43. The Ministry of Family and Consumer Affairs, Copenhagen.
4. Anonymous. 2008. A quantitative microbiological risk assessment on Salmonella in meat. 1. Source attribution for human salmonellosis from meat. EFSA J. 625:1-32.
5. Beloeil, P. A., P. Fravalo, C. Fablet, J. P. Jolly, E. Eveno, Y. Hascoet, C. Chauvin, G. Salvat, and F. Madec. 2004. Risk factors for Salmonella enterica subsp. enterica shedding by market-age pigs in French farrow-to-finish herds. Prev. Vet. Med. 63:103-120.
6. Berends, B. R., H. A. Urlings, J. M. Snijders, and F. Van Knapen. 1996. Identification and quantification of risk factors in animal management and transport regarding Salmonella spp. in pigs. Int. J. Food Microbiol. 30:37-53.
7. Berends, B. R., F. Van Knapen, D. A. Mossel, S. A. Burt, and J. M. Snijders. 1998. Salmonella spp. on pork at cutting plants and at the retail level and the influence of particular risk factors. Int. J. Food Microbiol. 44:207-217.
8. Berends, B. R., F. Van Knapen, J. M. Snijders, and D. A. Mossel. 1997. Identification and quantification of risk factors regarding Salmonella spp. on pork carcasses. Int. J. Food Microbiol. 36:199-206.
9. Bertrand, S., L. De Zutter, M. Vrints, C. Wildemauwe, N. Bottledoorn, K. Dierick, and J. Collard. 2008. Pork products and human salmonellosis: lessons learned from a national outbreak linked to the consumption of pork, p. 76. In First Belgian Symposium on Salmonella Research and Control in Pigs. Instituut voor de aanmoediging van Innovatie door Wetenschap en Technologie in Vlaanderen, Gent, Belgium.
10. Bolton, D. J., R. A. Pearce, J. J. Sheridan, I. S. Blair, D. A. McDowell, and D. Harrington. 2002. Washing and chilling as critical control points in pork slaughter hazard analysis and critical control point (HACCP) systems. J. Appl. Microbiol. 92:893-902.
11. 11. 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. (Pubitemid 26258083)
12. Botteldoorn, N., J. Durieux, B. Pochet, and K. Dierick. 2007. Reported food-borne outbreaks in Belgium in 2006, p. 124. In Twelfth Conference on Food Microbiology University of Liege, Liege, Belgium.
13. 13.Boudry,C.,N.Korsak,B.Jacob,G.Etienne,A.Théwis,andG.Daube.2002. EcologiedeSalmonelladansletubedigestifduporcàl'abattageeté tudedelacontaminationdescarcasses.Ann.Med.Vet.146:353-360.(Pubitemid36529327)
14. Brown, M. H., and A. C. Baird-Parker. 1982. The microbiological examination of meat. In M. H. Brown (ed.), Meat microbiology, p. 423-520. Applied Science Publishers, London.
15. Centre d'Etude et de Recherches Vétérinaires et Agro-chimiques. 2006. Salmonella serotypes analysed at the CODA-CERVA in 2005 evolution among poultry, cattle and pig isolates from 1992 to 2005 with results of antimicrobial resistance testing, p. 40. Centre d'Etude et de Recherches Vétérinaires et Agro-chimiques, Brussels.
16. Codex Alimentarius Commission. 1999. Principles and guidelines for the conduct of microbiological risk assessment. Codex Alimentarius Commission, Food and Agriculture Organization, World Health Organization, Geneva.
17. Couvert, O., S. Gaillard, N. Savy, P. Mafait, and I. Leguérinel. 2005. Survival curves of heated bacterial spores: effect of environmental factors on Weibull parameters. Int. J. Food Microbiol. 101:73-81.
18. CW3C. 2008. Animal slaughter in Wallonia. CW3C, Walloon Cell for carcass control, Liege, Belgium.
19. 19.Delhalle,L.,L.DeSadeleer,K.Bollaerts,F.Farnir,C.Saegerman,N.Korsak,J. Dewulf,D.DeZutter,andG.Daube.2008. RiskfactorsforSalmonellaandhygieneindicators inthetenlargestBelgianpigslaughterhouses.J.FoodProt.71:1320-1329. (Pubitemid351961720)
20. Delhalle, L., F. Farnir, and G. Daube. 2006. Development of a tool for Salmonella pork meat contamination modelling in Belgium, p. 162. In Eleventh Conference on Food Microbiology, Ghent, Belgium.
21. Delhalle, L., N. Korsak, and G. Daube. 2008. Salmonella dans la filière porcine: de l'abattoir au consommateur. L'essentiel du porc 3: 17-19.
22. Delhalle, L., C. Saegerman, F. Farnir, N. Korsak, D. Maes, W. Messens, L. De Sadeleer, L. De Zutter, and G. Daube. 2009. Salmonella surveillance and control at post harvest in the Belgian pork meat chain. Food Microbiol. 26:265-271.
23. Denagamage, T. N., A. M. O'Connor, J. M. Sargeant, A. Rajic, and J. D. McKean. 2007. Efficacy of vaccination to reduce Salmonella prevalence in live and slaughtered swine: a systematic review of literature from 1979 to 2007. Foodborne Pathog. Dis. 4:539-549.
24. Devriese, S., I. Huybrechts, M. Moreau, and H. Van Oyen. 2006. Enquête de consommation alimentaire Belge 2004, p. 877. Service d'Epidémiologie, Institut Scientifique de Santé Publique, Brussels.
25. European Food Safety Authority. 2007. The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents, Antimicrobial Resistance and Foodborne Outbreaks in the European Union in 2006. European Food Safety Authorities, Parma, Italy.
26. European Food Safety Authority. 2008. Report of the Task Force on Zoonoses Data Collection on the analysis of the baseline survey on the prevalence of Salmonella in slaughter pigs, Part A. EFSA J. 135: 1-111.
27. European Union. 2000. White paper on food safety. Commission of the European Communities, Brussels.
28. European Union. 2002. Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. Off. J. Eur. Union L 31:1-24.
29. European Union. 2004. Regulation (EC) No 852/2004 of the European Parliament of 29 April 2004 on the hygiene of foodstuffs. Off. J. Eur: Union 226/3-226/21.
30. European Union. 2004. Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Off. J. Eur. Union 001.001/1-59.
31. European Union. 2005. Règlement (EC) No 2073/2005 de la Commission du 15 novembre 2005 concernant les critères microbiologiques applicables aux denrées alimentaires. Off. J. Eur. Union 338/1-338/26.
32. FED Ho.Re.Ca. 2006. Guide for establishing a system of self monitoring in the HORECA sector. FED Ho.Re.Ca, Jambes, Belgium.
33. Food and Agriculture Organization-World Health Organization. 2002. Risk assessments of Salmonella in eggs and broiler chickens. Food and Agriculture Organization of the United Nations, Rome.
34. 34. Fosse, J., H. Seegers, and C. Magras. 2008. Foodborne zoonoses due to meat: a quantitative approach for a comparative risk assessment applied to pig slaughtering in Europe. Vet. Res. 39:1-16. (Pubitemid 350172904)
35. FPS Economy. 2007. Animal slaughter in Belgium. FPS Economy Directorate-general Statistics Belgium, Brussels.
36. Gellynck, X., W. Messens, D. Halet, K. Grijspeerdt, E. Hartnett, and J. Viaene. 2008. Economics of reducing Campylobacter at different levels within the Belgian poultry meat chain. J. Food Prot. 71:479-485.
37. Genovese, K. J., R. C. Anderson, R. B. Harvey, T. R. Callaway, T. L. Poole, T. S. Edrington, P. J. Fedorka-Cray, and D. J. Nisbet. 2003. Competitive exclusion of Salmonella from the gut of neonatal and weaned pigs. J Food Prot. 66:1353-1359.
38. Ghafir, Y., B. China, K. Dierick, L. De Zutter, and G. Daube, 2007. Hygiene indicator microorganisms for selected pathogens on beef, pork and poultry meats in Belgium. J. Food Prot. 70:104-112.
39. 39.Ghafir,Y.,B.China,N.Korsak,K.Dierick,J.M.Collard,C.Godard,L.DeZutter, andG.Daube.2005.Belgiansurveillanceplans- assesschangesinSalmonellaprevalenceinmeatatdifferentproductionstages.J.FoodProt. 68:2269-2277.(Pubitemid41630735)
40. Gill, C. O., and J. Bryant. 1993. The presence of Escherichia coli, Salmonella and Campylobacter in pig carcass dehairing equipment. Food Microbiol. 10:337-344.
41. Gledel, J. 1996. Le genre Salmonella, p. 62-79. In C. M. Bourgeois, J. F. Mescle, and J. Zueca (ed.), Microbiologie alimentaire: aspect microbiologique de la sécurité et de la qualité des aliments. Lavoisier, Paris.
42. 42. Hald, T., A. Wingstrand, M. Swanenburg, A. von Altrock, and B. M. Thorberg. 2003. The occurrence and epidemiology of Salmonella in European pig slaughterhouses. Epidemiol. Infect. 131:1187-1203. (Pubitemid 38195594)
43. Hill, A., T. England, E. Snary, A. Cook, L. Kelly, S. Evans, and M. Wooldridge. 2003. A 'farm-to-consumption' risk assessment for Salmonella Typhimurium in pigs. Veterinary Laboratories Agency, Weybridge.
44. Hurd, H. S., J. D. McKean, I. V. Wesley, and L. A. Karriker. 2001. The effect of lairage on Salmonella isolation from market swine. J. Food Prot. 64:939-944.
45. Institut technique du porc. 2000. Memento de l'éleveur de porc. Institut technique du porc, Paris.
46. International Commission on Microbiological Specifications for Foods. 1996. Microorganisms in foods: characteristics of microbial pathogens. Blackie Academic & Professional, London.
47. International Commission on Microbiological Specifications for Foods. 2005. Microorganisms in foods 6: microbial ecology of food commodities. Springer, New York.
48. 48. Jackson, V., I. S. Blair, D. A. McDowell, J. Kennedy, and D. J. Bolton. 2007. The incidence of significant foodborne pathogens in domestic refrigerators. Food Control 18:346-351. (Pubitemid 44472266)
49. Korsak, N. 2005. Mise au point et validation de méthodes de surveillance et de prévention de Salmonella dans une filière porcine intégrée, p. 353. Food Science Department, Liege University, Liège, Belgium.
50. Korsak, N., J. N. Degeye, G. Etienne, J. M. Beduin, B. China, Y. Ghafir, and G. Daube. 2006. Use of a serological approach for prediction of Salmonella status in an integrated pig production system. Int. J. Food Microbiol. 108:246-254.
51. 51.Korsak,N.,B.Jacob,B.Graven,G.Etienne,B.China,Y.Ghafir,andG.Daube.2003. Salmonellacontaminationofpigsandporkinanintegratedpigproductionsystem.J. FoodProt.66:1126-1133.(Pubitemid36844697)
52. 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 spp. via domestic kitchen surfaces. J. Food Prot. 67:1892-1903.
53. Le Roux, A., B. Minvielle, and E. Gault. 2008. Traitements assainissants localisés: intérêt du procédé «steam vacuum» dans la gestion des souillures fécales sur carcasses. Techni-Porc 31:15-18.
54. Leroy, B. 1999. Contribution to the risk assessment related to enterohaemorrhagic Escherichia coli 0157 in raw beef minced meat, p. 110. Food Science Department-Foods of Animal Origin, University of Liege, Liege, Belgium.
55. Lo Fo Wong, D. M., T. Hald, P. J. Van Der Wolf, and M. Swanenburg. 2002. Epidemiology and control measures for Salmonella in pigs and pork. Livest. Prod. Sei. 76:215-222.
56. McKellar, R. C. 2004. Modeling microbial responses in foods. CRC Press Inc., Boca Raton, FL.
57. 57.Medeiros,L.C.,V.N.Hillers,P.A.Kendall,andA.Mason.2001. Foodsafetyeducation:whatshouldwebeteaching-consumers'?J.Nutr.Educ.33:108-113. (Pubitemid33259280)
58. 58.Montville,R.,Y.Chen,andD.W.Schaffner.2001.Glovebarriers- bacterialcross-contaminationbetweenhands-food.JFoodProt.64:845-849. (Pubitemid32532749)
59. Montzey, S., and B. Minvielle. 2002. Specific treatment of pig carcasses by double singeing. Techni-Porc 25:25-29.
60. Mylius, S. D., M. J. Nauta, and A. H. Havelaar. 2007. Crosscontamination during food preparation: a mechanistic model applied to chicken-borne Campylobacter. Risk Anal. 27:803-813.
61. Nauta, M. J. 2001. A modular process risk model structure for quantitative microbiological risk assessment and its application in an exposure assessment of Bacillus cereus in a REPFED, p. 100. National Institute of Public Health and the Environment, Bilthoven, The Netherlands.
62. Nesbakken, T. 1994. The use of plastic bags to cover the rectum reduces the occurrence of Yersinia and Listeria in slaughtered pigs. Nor. Veterinaertidsskr. 106:491-492.
63. 63. 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. (Pubitemid 44287122)
64. 64. Nollet, N., D. Maes, L. De Zutter, L. Duchateau, K. Houf, K. Huysmans, H. Imberechts, R. Geers, A. de Kruif, and J. van Hoof. 2004. Risk factors for the herd-level bacteriologic prevalence of Salmonella in Belgian slaughter pigs. Prev. Vet. Med. 65:63-75. (Pubitemid 39348040)
65. 65.Ojha,S.,andM.Kostrzynska.2007. ApproachesforreducingSalmonellainporkproduction.J.FoodProt.70:2676-2694. (Pubitemid350086402)
66. Oosterom, J. 1991. Epidemiological studies and proposed preventive measures in the fight against human salmonellosis. Int. J. Food Microbiol. 12:41-51.
67. Palisade. 2004. @Risk advanced risk analysis for spreadsheet. Palisade, New York.
68. 68. Pearce, R. A., D. J. Bolton, J. J. Sheridan, D. A. McDowell, I. S. Blair, and D. Harrington. 2004. Studies to determine the critical control points in pork slaughter hazard analysis and critical control point systems. Int. J. Food Microbiol. 90:331-339. (Pubitemid 38147477)
69. Rahkio, M., H. Korkeala, I. Sippola, and M. Peltonen. 1992. Effect of pre-scalding brushing on contamination level of pork carcasses during the slaughtering process. Meat Sei. 32:173-183.
70. Rajkowski, K. T., S. Eblen, and C. Laubauch. 1998. Efficacy of washing and sanitizing trailers used for swine transport in reduction of Salmonella and Escherichia coli. J. Food Prot. 61:31-35.
71. Ranta, J., P. Tuominen, E. Rautiainen, and R. Miajala. 2004. Salmonella in pork production in Finland-a quantitative risk assessment, p. 104. National Veterinary and Food Research Institute, Helsinki, Finland.
72. 72. Ribbens, S., J. Dewulf, D. Maes, F. Koenen, K. Mintiens, L. Desadeleer, A. de Kruif, and D. Maes. 2008. A survey on biosecurity and management practices in Belgian pig herds. Prev. Vet. Med. 83: 228-241. (Pubitemid 351192115)
73. 73.Rivas,T.,J.A.Vizcaino,andF.J.Herrera.2000. MicrobialcontaminationofcarcassesandequipmentfromanIberianpigslaughterhouse.J. FoodProt.63:1670-1675.(Pubitemid32192010)
74. Sannaa, M. 2002. Microbiologie prévisionelle: principaux modèles utilisés en appréciation quantitative de risque. Epidemiol. Santé Anim. 41:169-177.
75. Schwartz, K. J. 1999. Salmonellosis, p. 535-551. In B. E. Straw, S. d'Allaire, W. L. Mengeling, and D. J. Taylor (ed.), Diseases of swine, 8th ed. Blackwell Science, Oxford.
76. Scientific Institute of Public Health. 2007. Annual report on human Salmonella and Shigella in Belgium 2006. National Reference Center for Salmonella and Shigella Scientific Institute of Public Health, Brussels.
77. Scott, E. 1999. Hygiene issues in the home. Am. J. Infect. Control 27: S22-S25.
78. 78.Scott,E.2003.Foodsafetyandfoodbornediseasein21stcenturyhomes.Can.J. Infect.Dis.14:277-280.(Pubitemid37428980)
79. Sorqvist, S., and M. L. Danielsson-Tham. 1990. Survival of Campylobacter, Salmonella and Yersinia spp. in scalding water used at pig slaughter. Fleischwirtschaft 70:1451-1454.
80. 80.Spescha,C.,R.Stephan,andC.Zweifel.2006. Microbiologicalcontaminationofpigcarcassesat differentstagesofslaughterintwoEuropeanUnion-approvedabattoirs.J.FoodProt.69: 2568-2575.(Pubitemid44786826)
81. SPF economy. 2007. Population et ménages-Population totale et belge, p. 280. Direction générale Statistique et Information économique, Brussels.
82. 82.Swanenburg,M.,B.R.Berends,H.A.P.Urlings,J.M.A.Snijders,andF.vanKnapen. 2001.EpidemiologicalinvestigationsintothesourcesofSalmonellacontaminationofpork. Berl.Munch.Tierarztl.Wochenschr.114:356-359.(Pubitemid32943725)
83. Swanenburg, M., H. A. P. Urlings, D. A. Keuzenkamp, and J. M. A. Snijders. 2001. Salmonella in the lairage of pig slaughterhouses. J. Food Prot. 64:12-16.
84. Test Achats. 2003. Temperature in food products, p. 8-9. In Test achats, vol.464. Brussels.
85. Uniporc. 2008. Taux de muscles des pièces-classement par porc. UNIPORC OUEST, Plerin, France.
86. Valkenburgh, S., R. van Oosterom, O. Stenvers, M. Aalten, M. Braks, B. Schimmer, A. van de Giessen, W. van Pelt, and M. Langelaar. 2007. Zoonoses and zoonotic agents in humans, food, animals and feed in the Netherlands 2003-2006, p. 140. Rijksinstituut voor Volksgezondheid en Milieu, Bilthoven, The Netherlands.
87. van der Gaag, M. A. 2004. Epidemiological and economic simulation of Salmonella control in the pork supply chain. Ph.D. thesis. Wageningen University, Wageningen, The Netherlands.
88. van Kreijl, C. F., A. G. A. C. Knaap, and J. M. A. Raaij. 2006. Our food, healthy diet and safe food in The Netherlands. RIVM Rapport 270555009, p. 364. Rijksinstituut voor Volksgezondheid en Milieu, Bilthoven, The Netherlands.
89. Voetsch, A. C., T. J. Van Gilder, F. J. Angulo, M. M. Farley, S. Shallow, R. Marcus, P. R. Cieslak, V. C. Deneen, and R. V. Tauxe. 2004. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin. Infect. Dis. 38(Suppl. 3):S127-S134.
90. Vose, D. 2000. Risk analysis: a quantitative guide. John Wiley & Sons Inc. Chichester, UK.
91. Vose, D. 2005. Model Assist Advanced for @Risk. Vose Consulting, Risk Thinking Ltd, Ghent, Belgium.
92. Witvliet, M. H. 2008. Vaccination as a tool to reduce Salmonella infection in pigs, p. 27-30. In Proceedings of the First Belgian Symposium on Salmonella Research and Control in Pigs, Ghent, Belgium.