Tracking the Salmonella status of pigs and pork from lairage through the slaughter process in the republic of Ireland

Journal of Food Protection

Volumn 73, Issue 12, 2010, Pages 2148-2160

  Duggan, S J ^a   Mannion, C ^b   Prendergast, D M ^a   Leonard, N ^b   Fanning, S ^b   Gonzales Barron, U ^b   Egan, J ^c   Butler, F ^b   Duffy, G ^a  

^a ASHTOWN FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c CENTRAL VETERINARY RESEARCH LABORATORY   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROBACTERIACEAE; SALMONELLA; SALMONELLA TYPHIMURIUM; SUIDAE;

EID: 78650506111     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-73.12.2148     Document Type: Article

References (62)

1. Anonymous. 2006. Opinion of the Scientific Panel on Biological Hazards (BIOHAZ) related to "Risk assessment and mitigation options of Salmonella in pig production." Available at: http://www.efsa.europa.eu/EFSA/efsa- locale-1178620753812-1178620776028.htm. Accessed 15 August 2009.
2. Anonymous. 2007. The Community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2006. EFSA J. 130:2-352.
3. Anonymous. 2007. Report on zoonoses in Ireland 2005. Available at: http://www.fsai.ie/publications/index.asp#reports. Accessed 15 August 2009.
4. Anonymous. 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 B. EFSA J. 206:1-111.
5. Berends, B. R., F. Van Knapen, J. M. A. Snijders, and D. A. A. Mossel. 1997. Identification and quantification of risk factors regarding Salmonella spp. on pork carcasses. Int. J. Food Microbiol. 36:199-206. (Pubitemid 27361711)
6. Botteldoorn, N., N. Heyndrickx, N. Rijpens, K. Grijspeerdt, and L. Herman. 2003. Salmonella on pig carcasses: positive pigs and cross contamination in the slaughterhouse. J. Appl. Microbiol. 95:891-903. (Pubitemid 37357371)
7. Boughton, C., J. Egan, G. Kelly, B. Markey, and N. Leonard. 2007. Quantitative examination of Salmonella spp. in the lairage environment of a pig abattoir. Foodborne Pathog. Dis. 4(1). DOI: 10.1089/fpd.2006.57. (Pubitemid 46466587)
8. Boughton, C., J. Egan, G. Kelly, B. Markey, and N. Leonard. 2007. Rapid infection of pigs following exposure to environments contaminated with different levels of Salmonella Typhimurium. Foodborne Pathog. Dis. 4(1). DOI: 10.1089/fpd.2006.58. (Pubitemid 46466588)
9. Boyen, F., F. Haesebrouck, D. Maes, F. Van Immerseel, R. Ducatelle, and F. Pasmans. 2008. Non-typhoidal Salmonella infections in pigs: a closer look at epidemiology, pathogenesis and control. Vet. Microbiol. 130:1-19.
10. Brunn, T., G. Sorensen, L. P. Forshell, T. Jensen, K. Nygard, G. Kapperud, B. A. Lindstedt, T. Berglund, A. Wingstrand, R. F. Petersen, L. Muller, C. Kjelso, S. Ivarsson, M. Hjertqvist, S. Lofdahl, and S. Ethelberg. 2009. An outbreak of Salmonella Typhimurium infections in Denmark, Norway and Sweden, 2008. Eurosurveillance 14(10):1-6.
11. Buchholz, U., B. Brodhun, S. O. Brockmann, C. M. Dreweck, R. Prager, H. Tschape, and A. Ammon. 2005. An outbreak of Salmonella München in Germany associated with raw pork. J. Food Prot. 68:273-276. (Pubitemid 40218130)
12. Casey, P. G., D. Butler, G. E. Gardiner, M. Tangney, P. Simpson, P. G. Lawlor, C. Stanton, R. P. Ross, C. Hill, and G. F. Fitzgerald. 2004. Salmonella carriage in an Irish pig herd: correlation between serological and bacteriological detection methods. J. Food Prot. 67: 2797-2800. (Pubitemid 39623360)
13. Catarame, T. M. G., K. A. O'Hanlon, D. A. McDowell, I. S. Blair, and G. Duffy. 2006. Comparison of a real time polymerase chain reaction assay with a culture method for the detection of Salmonella in retail meat samples. J. Food Saf. 26:1-15.
14. Childers, A. B., and E. E. Keahey. 1977. Reduction of Salmonella and fecal contamination of pork during swine slaughter. J. Am. Vet. Med. Assoc. 171:1161-1164.
15. Davies, R. H., R. Dalziel, J. C. Gibbens, J. W. Wilesmith, J. M. Ryan, S. J. Evans, C. Byrne, G. A. Paiba, S. J. S. Pascoe, and C. J. Teale. 2004. National survey of Salmonella in pigs, cattle and sheep at slaughter in Great Britain (1999-2000). J. Appl. Microbiol. 96:750-760. (Pubitemid 38437834)
16. Davies, R. H., P. J. Heath, S. M. Coxon, and A. R. Sayers. 2003. Evaluation of the use of pooled serum, pooled muscle tissue fluid (meat juice) and pooled faeces for monitoring pig herds for Salmonella. J. Appl. Microbiol. 95:1016-1025.
17. de Man, J. C. 1983. MPN tables, corrected. Eur. J. Appl. Microbiol. 17:301-305.
18. Farzan, A., R. M. Friendship, and C. E. Dewey. 2007. Evaluation of enzyme-linked immunosorbent assay (ELISA) tests and culture for determining Salmonella status of a pig herd. Epidemiol. Infect. 135: 238-244. (Pubitemid 46322061)
19. Fedorka-Cray, P. J., L. Collins Kelley, T. J. Stabel, J. T. Gray, and J. A. Laufer. 1995. Alternate routes of invasion may affect pathogenesis of Salmonella Typhimurium in swine. Infect. Immun. 63:2658-2664.
20. Giovannacci, I., S. Queguiner, C. Ragimbeau, G. Salvat, J. L. Vendeuvre, V. Carlier, and G. Ermel. 2001. Tracing of Salmonella spp. in two pork slaughter and cutting plants using serotyping and macrorestriction genotyping. J. Appl. Microbiol. 90:131-147. (Pubitemid 32150303)
21. Gonzales Barron, U., I. Soumpasis, F. Butler, D. Prendergast, S. Duggan, and G. Duffy. 2009. Estimation of prevalence of Salmonella on pig carcasses and pork cut joints, using a quantitative risk assessment model aided by meta-analysis. J. Food Prot. 72:274-285.
22. 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)
23. Hurd, H. S., J. K. Gailey, J. D. McKean, and R. W. Griffith. 2005. Variable abattoir conditions affect Salmonella enterica prevalence and meat quality in swine and pork. Foodborne Pathog. Dis. 2: 77-81.
24. Hurd, H. S., J. D. McKean, R. D. Griffith, and M. H. Rostagno. 2003. Estimation of the Salmonella enterica prevalence in finishing swine. Epidemiol. Infect. 132:127-135.
25. 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.
26. Jansen, A., C. Frank, R. Prager, H. Oppermann, and K. Stark. 2005. Nation-wide outbreak of Salmonella Give in Germany, 2004. Z. Gastroenterol. 43:707-713. (Pubitemid 41233457)
27. Jansen, A., C. Frank, and K. Stark. 2007. Pork and pork products as a source for human salmonellosis in Germany. Berl. Muench. Tieraerztl. Wochenschr. 120(7-8):340-346. (Pubitemid 47074898)
28. Käsbohrer, A., D. Protz, R. Helmuth, K. Nöckler, T. Blaha, F. J. Conraths, and L. Geue. 2000. Salmonella in slaughter pigs of German origin: an epidemiological study. Eur. J Epidemiol. 16:141-146. (Pubitemid 30322119)
29. Keenliside, J., G. Gensler, R. King, M. McFall, and L. Goonewardene. 2005. Prevalence and relatedness of Salmonella spp. in a Canadian abattoir, p. 38-41. In Proceedings of the 6th International Symposium on Epidemiology and Control of Salmonella in Pork, Rohnert Park, CA, 6 to 9 September 2005.
30. 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.
31. Kranker, S., L. Alban, J. Boes, and J. Dahl. 2003. Longitudinal study of Salmonella enterica serotype Typhimurium infection in three Danish farrow-to-finish swine herds. J. Clin. Microbiol. 41:2282-2288. (Pubitemid 36712424)
32. Larsen, S. T., H. S. Hurd, J. D. McKean, R. W. Griffith, and L. V. Wesley. 2004. Effect of short-term lairage on the prevalence of Salmonella enterica in cull sows. J. Food Prot. 67:1489-1493.
33. Little, C. L., J. F. Richardson, R. J. Owen, E. de Pinna, and E. J. Threlfall. 2008. Campylobacter and Salmonella in raw red meats in the United Kingdom: prevalence, characterization and antimicrobial resistance pattern, 2003-2005. Food Microbiol. 25:538-543.
34. Lo Fo Wong, D. M. A., J. Dahl, A. Wingstrand, P. J. van der Wolf, A. von Altrock, and B. M. Thorberg. 2004. A European longitudinal study in Salmonella seronegative-and seropositive-classified finishing pig herds. Epidemiol. Infect. 132:903-914. (Pubitemid 39307348)
35. Lo Fo Wong, D. M. A., T. Hald, P. J. van der Wolf, and M. Swanenburg. 2002. Epidemiology and control measures for Salmonella in pigs and pork. Livest. Prod. Sci. 76:215-222. (Pubitemid 35008647)
36. Luzzi, I., P. Galetta, M. Massari, C. Rizzo, A. M. Dionisi, E. Filetici, A. Cawthorne, A. Tozzi, M. Argentieri, S. Bilei, L. Busani, C. Gnesivo, A. Pendenza, A. Piccoli, P. Napoli, L. Loffredo, M. O. Trinito, E. Santarelli, and M. L. Ciofi degli Atti. 2007. An Easter outbreak of Salmonella Typhimurium DT 104A associated with traditional pork salami in Italy. Eurosurveillance 12(4):E11-E12.
37. Magistrali, C., A. M. Dionisi, P. De Curtis, L. Cucco, O. Vischi, S. Scuota, A. Zicavo, and G. Pezzotti. 2008. Contamination of Salmonella spp. in a pig finishing herd, from the arrival of the animals to the slaughterhouse. Res. Vet. Sci. 85:204-207.
38. Mannion, C., J. Egan, P. Lynch, S. Fanning, and N. Leonard. 2008. An investigation into the efficacy of washing trucks following transportation of pigs - a Salmonella perspective. Foodborne Pathog. Dis. 5(3). DOI: 10.1089/fpd.2007.0069. (Pubitemid 351873421)
39. Marjatta Rahkio, T., and H. J. Korkeala. 1997. Airborne bacteria and carcass contamination in slaughterhouses. J. Food Prot. 60:38-42.
40. McDowell, S. W. J., R. Porter, R. Madden, B. Cooper, and S. D. Neill. 2007. Salmonella in slaughter pigs in Northern Ireland: prevalence and use of statistical modelling to investigate sample and abattoir effects. Int. J. Food Microbiol. 118:116-125. (Pubitemid 47371029)
41. Mossong, J., P. Marques, C. Ragimbeau, P. Humerty-Krau, S. Losch, G. Meyer, G. Moris, C. Strottner, W. Rabsch, and F. Schneider. 2007. Outbreaks of monophasic Salmonella enterica serovar 4,[5],12:i:-in Luxembourg, 2006. Eurosurveillance 12(6):E11-E12.
42. Murase, T., M. Yamada, T. Muto, A. Matsushima, and S. Yamai. 2000. Fecal excretion of Salmonella enterica serovar Typhimurium following a food-borne outbreak. J. Clin. Microbiol. 38:3495-3497.
43. Nielsen, B., D. Baggensen, F. Bager, J. Haugegaard, and P. Lind. 1995. The serological response to Salmonella serovars Typhimurium and Infantis in experimentally infected pigs. The time course followed with an indirect anti-LPS ELISA and bacteriological examinations. Vet. Microbiol. 47:205-218.
44. Noel, H., M. Dominguez, F. X. Weill, A. Brisbois, C. Duchazeaubeneix, A. Kerouantou, G. Delmas, N. Pihier, and E. Couturier. 2006. Outbreak of Salmonella enterica serotype Manhattan infection associated with meat products, France, 2005. Eurosurveillance 11(11):270-273.
45. 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)
46. Nowak, B., T. von Muffling, S. Chaunchom, and J. Hartung. 2007. Salmonella contamination in pigs at slaughter and on the farm: a field study using an antibody ELISA test and a PCR technique. Int. J. Food Microbiol. DOI: 10.1016/j.ijfoodmicro.2006.10.045. (Pubitemid 46415643)
47. Pearce, R. A., and D. J. Bolton. 2005. Excision vs sponge swabbing - a comparison of methods for the microbiological sampling of beef, pork and lamb carcasses. J. Appl. Microbiol. 98:896-900. (Pubitemid 40477266)
48. Prendergast, D. M., S. J. Duggan, S. Fanning, M. Cormican, U. Gonzales-Barron, F. Butler, and G. Duffy. 2008. Prevalence and numbers of Salmonella spp. and Enterobacteriaceae on pork cuts in abattoirs in the Republic of Ireland. J. Appl. Microbiol. 105:1209-1219.
49. Prendergast, D. M., S. J. Duggan, U. Gonzales-Barron, S. Fanning, F. Butler, M. Cormican, and G. Duffy. 2009. Prevalence, numbers and characterisation of Salmonella spp. on Irish retail pork. Int. J. Food Microbiol. 131:233-239.
50. Proux, K., R. Cariolet, P. Fravalo, C. Houdayer, A. Keranflech, and F. Madec. 2001. Contamination of pigs by nose-to-nose contact or airborne transmission of Salmonella Typhimurium. Vet. Res. 32:591-600. (Pubitemid 34013522)
51. Rostagno, M. H., H. S. Hurd, J. D. McKean, C. J. Ziemer, J. K. Gailey, and R. C. Leite. 2003. Preslaughter holding environment in pork plants is highly contaminated with Salmonella enterica. Appl. Environ. Microbiol. 69:4489-4494.
52. Schmidt, P. L., A. M. O'Connor, J. D. McKean, and H. S. Hurd. 2004. The association between cleaning and disinfection of lairage pens and the prevalence of Salmonella enterica in swine at harvest. J. Food Prot. 67:1384-1388.
53. Small, A., C.-A. Reid, S. M. Avery, N. Karabasil, C. Crowley, and S. Buncic. 2002. Potential for the spread of Escherichia coli O157, Salmonella, and Campylobacter in the lairage environment at abattoirs. J. Food Prot. 65:931-936. (Pubitemid 34609254)
54. Sorensen, L. L., L. Alban, B. Nielsen, and J. Dahl. 2004. The correlation between Salmonella serology and isolation of Salmonella in Danish pigs at slaughter. Vet. Microbiol. 101:131-141. (Pubitemid 38692770)
55. Swanenburg, M., B. R. Berends, H. A. P. Urlings, J. M. A. Snijders, and F. van Knapen. 2001. Epidemiological investigations into the sources of Salmonella contamination of pork. Berl. Muench. Tieraerztl. Wochenschr. 114:356-359. (Pubitemid 32943725)
56. Swanenburg, M., H. A. P. Urlings, J. M. A. Snijders, D. A. Keuzenkamp, and F. van Knapen. 2001. Salmonella in slaughter pigs: prevalence, serotypes and critical control points during slaughter in two slaughterhouses. Int. J. Food Microbiol. 70:243-254. (Pubitemid 33016338)
57. Swanenburg, M., P. J. van der Wolf, H. A. P. Urlings, J. M. A. Snijders, and F. van Knapen. 2001. Salmonella in slaughter pigs: the effect of logistic slaughter procedures of pigs on the prevalence of Salmonella in pork. Int. J. Food Microbiol. 70:231-242. (Pubitemid 33016337)
58. Thouberg, B. M., and A. Engvall. 2001. Incidence of Salmonella in five Swedish slaughterhouses. J. Food Prot. 64:542-545. (Pubitemid 32368280)
59. Trkov, M., and G. Avgustin. 2003. An improved 16S rRNA based PCR method for the specific detection of Salmonella enterica. Int. J. Food Microbiol. 80:67-75.
60. Valdezate, S., A. Vidal, S. Herrera-Leon, J. Pozo, P. Rubio, A. Usera, A. Carvajal, and M. Aurora Echeita. 2005. Salmonella Derby clonal spread from pork. Emerg. Infect. Dis. 11:694-698. (Pubitemid 40586392)
61. Vieira-Pinto, M., P. Temudo, and C. Martins. 2005. Occurrence of Salmonella in the ileum, ileocolic lymph nodes, tonsils, mandibular lymph nodes and carcasses of pigs slaughtered for consumption. J. Vet. Med. Sci. 52:476-481. (Pubitemid 44922240)
62. Vieira-Pinto, M., R. Tenreiro, and C. Martins. 2006. Unveiling contamination sources and dissemination routes of Salmonella sp. In pigs at a Portuguese slaughterhouse through macrorestriction profiling by pulsed-field gel electrophoresis. Int. J. Food Microbiol. 110:77-84. (Pubitemid 44056089)