Contamination of food products with Mycobacterium avium paratuberculosis: A systematic review

Journal of Applied Microbiology

Volumn 107, Issue 4, 2009, Pages 1061-1071

  Eltholth, M M ^a   Marsh, V R ^a   Van Winden, S ^a   Guitian, F J ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Contamination; Dairy products; Meat products; Mycobacterium paratuberculosis; Processing; Systematic review

Indexed keywords

DAIRIES; DAIRY PRODUCTS; MEATS; PASTEURIZATION; SALES;

CROHN DISEASE; HUMAN EXPOSURES; MEAT PRODUCTS; MYCOBACTERIA PARATUBERCULOSIS; PARATUBERCULOSIS; PASTEURIZED MILK; PROCESSING; PRODUCTION CHAIN; RAW MILK; SYSTEMATIC REVIEW;

CONTAMINATION;

BACTERIUM; CATTLE; DISEASE TRANSMISSION; FOOD POISONING; FOOD PROCESSING; LITERATURE REVIEW; MEAT; PUBLIC HEALTH;

BEEF; CROHN DISEASE; DAIRY PRODUCT; FARM ANIMAL; FOOD CONTAMINATION; FOOD INDUSTRY; FOOD PROCESSING; GOAT; HEAT TREATMENT; MILK; MYCOBACTERIUM PARATUBERCULOSIS; NONHUMAN; PARATUBERCULOSIS; PASTEURIZATION; PREVALENCE; RAW MEAT; REVIEW; SHEEP; SYSTEMATIC REVIEW;

ANIMALIA; MYCOBACTERIUM AVIUM; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS;

EID: 70349161098     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2009.04286.x     Document Type: Review

References (84)

1. Abubakar, I., Myhill, D., Aliyu, S.H. Hunter, P.R. (2008) Detection of Mycobacterium avium subspecies paratuberculosis from patients with Crohn's disease using nucleic acid-based techniques: a systematic review and meta-analysis. Inflamm Bowel Dis 14, 401 410.
2. Adkin, A., Hartnett, E., Jordan, L., Newell, E. Davison, H. (2006) Use of a systematic review to assist the development of Campylobacter control strategies in broilers. J Appl Microbiol 100, 306 315.
3. Antognoli, M.C., Garry, F.B., Hirst, H.L., Lombard, J.E., Dennis, M.M., Gould, D.H. Salman, M.D. (2008) Characterization of Mycobacterium avium subspecies paratuberculosis disseminated infection in dairy cattle and its association with antemortem test results. Vet Microbiol 127, 300 308.
4. Austin, J.W. Bergeron, G. (1995) Development of bacterial biofilms in dairy processing lines. J Dairy Res 62, 509 519.
5. Ayele, W.Y., Bartos, M., Svastova, P. Pavlik, I. (2004) Distribution of Mycobacterium avium subspecies paratuberculosis in organs of naturally infected bull-calves and breeding bulls. Vet Microbiol 103, 209 217.
6. Ayele, W.Y., Svastova, P., Roubal, P., Bartos, M. Pavlik, I. (2005) Mycobacterium avium subspecies paratuberculosis cultured from locally and commercially pasteurized cow's milk in the Czech Republic. Appl Environ Microbiol 71, 1210 1214.
7. Bell, R.G. (1997) Distribution and sources of microbial contamination on beef carcasses. J Appl Microbiol 82, 292 300.
8. Bell, R.G. Hathaway, S.C. (1996) The hygienic efficiency of conventional and inverted lamb dressing systems. J Appl Bacteriol 81, 225 234.
9. Biss, M.E. Hathaway, S.C. (1995) Microbiological and visible contamination of lamb carcasses according to preslaughter presentation status: implications for HACCP. J Food Prot 58, 776 783.
10. Biss, M.E. Hathaway, S.C. (1996) The effect of different on-line dressing practices on microbiological and visible contamination of lamb carcasses. NZ Vet J 44, 55 60.
11. Biss, M.E. Hathaway, S.C. (1998) A HACCP-based approach to hygienic slaughter and dressing of lamb carcasses. N Z Vet J 46, 167 172.
12. Boelaert, F., Walravens, K., Biront, P., Vermeersch, J.P., Berkvens, D. Godfroid, J. (2000) Prevalence of paratuberculosis (JD) in the Belgian cattle population. Vet Microbiol 77, 269 281.
13. Brady, C., O'Grady, D., O'Meara, F., Egan, J. Bassett, H. (2008) Relationships between clinical signs, pathological changes and tissue distribution of Mycobacterium avium subspecies paratuberculosis in 21 cows from herds affected by Johne's disease. The Vet Rec 162, 147 152.
14. Castillo, A., Lucia, L.M., Goodson, K.J., Savell, J.W. Acuff, G.R. (1998) Comparison of water wash, trimming, and combined hot water and lactic acid treatments for reducing bacteria of fecal origin on beef carcasses. J Food Prot 61, 823 828.
15. Cetinkaya, B., Erdogan, H.M. Morgan, K.L. (1998) Prevalence, incidence and geographical distribution of JD in cattle in England and the Welsh borders. The Vet Rec 143, 265 269.
16. Chamberlin, W., Graham, D.Y., Hulten, K., El-Zimaity, H.M.T., Schwartz, M.R., Naser, S., Shafran, I. El-Zaatari, F.A.K. (2001) Review article: Mycobacterium avium subsp. paratuberculosis as one cause of Crohn's disease. Alim Pharmac Ther 15, 337 346.
17. Clark, D.L. Jr., Anderson, J.L., Koziczkowski, J.J. Ellingson, J.L.E. (2006) Detection of Mycobacterium avium ssp. paratuberculosis genetic components in retail cheese curds purchased in Wisconsin and Minnesota by PCR. Mol Cell Probes 20, 197 202.
18. Cocito, C., Gilot, P., Coene, M., de Kesel, M., Poupart, P. Vannuffel, P. (1994) Paratuberculosis. Clin Microbial Rev 7, 328 345.
19. Collins, M.T. (1997) Mycobacterium paratuberculosis: a potential food-borne pathogen? J Dairy Sci 80, 3445 3448.
20. Cook, D.J., Mulrow, C.D. Haynes, R.B. (1997) Systematic reviews: synthesis of best evidence for clinical decisions. Ann Int Med 126, 367 380.
21. Corti, S. Stephan, R. (2002) Detection of Mycobacterium avium ssp. paratuberculosis specific IS900 insertion sequences in bulk-tank milk samples obtained from different regions throughout Switzerland. BMC Microbiol 2, 15.
22. CRD (2001) Center for reviews and dissemination guidance document-undertaking systematic reviews of research on effectiveness. CRD Report Number 4, 2nd edn, March 2001. Available at http://www.york.ac.uk/inst/crd/ report4.htm.
23. Dargatz, D.A., Byrum, B.A., Hennager, S.G., Barber, L.K., Kopral, C.A., Wagner, B.A. Wells, S.J. (2001) Prevalence of antibodies against Mycobacterium avium ssp. paratuberculosis among beef cow-calf herds. J Am Vet Med Assoc 219, 497 501.
24. Dieguez, F.J., Arnaiz, I., Sanjuan, M.L., Vilar, M.J., Lopez, M. Yus, E. (2007) Prevalence of serum antibodies to Mycobacterium avium ssp. paratuberculosis in cattle in Galicia (northwest Spain). Prev Vet Med 82, 321 326.
25. Djonne, B., Jensen, M.R., Grant, I.R. Holstad, G. (2003) Detection by immunomagnetic PCR of Mycobacterium avium ssp. paratuberculosis in milk from dairy goats in Norway. Vet Microbiol 92, 135 143.
26. Donaghy, J.A., Totton, N.L. Rowe, M.T. (2004) Persistence of Mycobacterium paratuberculosis during manufacture and ripening of cheddar cheese. Appl Environ Microbiol 70, 4899 4905.
27. Donaghy, J.A., Linton, M., Patterson, M.F. Rowe, M.T. (2007) Effect of high pressure and pasteurization on Mycobacterium avium ssp. paratuberculosis in milk. Lett Appl Microbiol 45, 154 159.
28. Dreier, S., Khol, J.L., Stein, B., Fuchs, K., Gutler, S. Baumgartner, W. (2006) Serological, bacteriological and molecularbiological survey of paratuberculosis (JD) in Austrian cattle. J Vet Med 53, 477 481.
29. Ellingson, J.L., Anderson, J.L., Koziczkowski, J.J., Radcliff, R.P., Sloan, S.J., Allen, S.E. Sullivan, N.M. (2005) Detection of viable Mycobacterium avium ssp. paratuberculosis in retail pasteurized whole milk by two culture methods and PCR. J Food Prot 68, 966 972.
30. Feller, M., Huwiler, K., Stephan, R., Altpeter, E., Shang, A., Furrer, H., Pfyffer, G.E., Jemmi, T. et al. (2007) Mycobacterium avium subspecies paratuberculosis and Crohn's disease: a systematic review and meta-analysis. Lancet Infect Dis 7, 607 613.
31. Gao, A., Mutharia, L., Chen, S., Rahn, K. Odumeru, J. (2002) Effect of pasteurization on survival of Mycobacterium avium ssp. paratuberculosis in milk. J Dairy Sci 85, 3198 3205.
32. Gill, C.O., McGinnis, J.C. Badoni, M. (1996) Use of total of Escherichia coli counts to assess the hygienic characteristics of a beef carcass dressing process. Int J Food Microbiol 31, 181 196.
33. Gorman, B.M, Morgan, J.B., Sofos, J.N. Smith, G.C. (1995) Microbiological and visual effects of trimming and/or spray washing for removal of faecal material from beef. J Food Prot 58, 984 989.
34. Grant, I.R. (2003) Mycobacterium paratuberculosis and milk. Acta Vet Scand 44, 261 266.
35. Grant, I.R. (2006) Mycobacterium avium ssp. paratuberculosis in foods: current evidence and potential consequences. Int J Dairy Technol 59, 112 117.
36. Grant, I.R., O'Riordan, L.M., Ball, H.J. Rowe, M.T. (2001) Incidence of Mycobacterium avium ssp. paratuberculosis in raw sheep and goats' milk in England, Wales and Northern Ireland. Vet Microbiol 79, 123 131.
37. Grant, I.R., Ball, H.J. Rowe, M.T. (2002) Incidence of Mycobacterium paratuberculosis in bulk raw and commercially pasteurized cows' milk from approved dairy processing establishments in United Kingdom. Appl Environ Microbiol 68, 2428 2435.
38. Grant, I.R., Williams, A.G., Rowe, M.T. Muir, D.D. (2005a) Investigating of the impact of simulated commercial centrifugation and microfiltration conditions on levels of Mycobacterium avium ssp. paratuberculosis in milk. Int J Dairy Technol 58, 138 142.
39. Grant, I.R., Williams, A.G., Rowe, M.T. Muir, D.D. (2005b) Efficacy of various pasteurization time-temperature conditions in combination with homogenization on inactivation of Mycobacterium avium ssp. paratuberculosis in milk. Appl Environ Microbiol 71, 2853 2861.
40. Hadley, P.J., Holder, J.S. Hinton, M.H. (1997) Effects of fleece soiling and skinning method on the microbiology of sheep carcases. Vet Rec 140, 570 574.
41. Hendrick, S., Duffield, T., Leslie, K., Lissemore, K., Archambault, M. Kelton, D. (2005) The prevalence of milk and serum antibodies to Mycobacterium avium ssp. paratuberculosis in dairy herds in Ontario. Can Vet J 46, 1126 1129.
42. Hermon-Taylor, J. Bull, T. (2002) Crohn's disease caused by Mycobacterium avium spp. paratuberculosis: a public health tragedy whose resolution is long overdue. J Med Microbiol 51, 3 6.
43. Hill, B.B., West, M. Brock, K.V. (2003) An estimated prevalence of JD in a subpopulation of Alabama beef cattle. J Vet Diagn Invest 15, 21 25.
44. Hines, S.A., Buergelt, C.D., Wilson, J.H. Bliss, E.L. (1987) Disseminated Mycobacterium paratuberculosis infection in a cow. J Am Vet Med Assoc 190, 681 683.
45. Hirst, H.L., Garry, F.B., Morley, P.S., Salman, M.D., Dinsmore, R.P., Wagner, B.A., McSweeney, K.D. Goodell, G.M. (2004) Seroprevalence of Mycobacterium avium ssp. paratuberculosis infection among dairy cows in Colorado and herd-level risk factors for seropositivity. J Am Vet Med Asso 225, 97 101.
46. Ikonomopoulos, J., Pavlik, I., Bartos, M., Svastova, P., Ayele, W.Y., Roubal, P., Lukas, J., Cook, N. et al. (2005) Detection of Mycobacterium avium ssp. paratuberculosis in retail cheeses from Greece and the Czech Republic. Appl Environ Microbiol 71, 8934 8936.
47. James, S.D. (1995) Susceptibility of pre-evisceration washed beef carcasses to contamination by Escherichia coli O157 : H7 and Salmonellae. J Food Prot 58, 1065 1068.
48. Jaravata, C.V., Smith, W.L., Rensen, G.J., Ruzante, J. Cullor, J.S. (2007) Survey of ground beef for the detection of Mycobacterium avium paratuberculosis. Foodborne Pathog Dis 4, 103 106.
49. Kochevar, S.L., Sofos, J.N., LeValley, S.B. Smith, G.C. (1997) Effect of water temperature, pressure and chemical solution on removal of faecal material and bacteria from lamb adipose tissue by spray-washing. Meat Science 45, 377 388.
50. Lambeth, C., Reddacliff, L.A., Windsor, P., Abbott, K.A., McGregor, H. Whittington, R.J. (2004) Intrauterine and transmammary transmission of Mycobacterium avium ssp. paratuberculosis in sheep. Aus Vet J 82, 504 508.
51. McDonald, W.L., O'Riley, K.J., Schroen, C.J. Condron, R.J. (2005) Heat inactivation of Mycobacterium avium ssp. paratuberculosis in milk. Appl Environ Microbiol 71, 1785 1789.
52. Meadus, W.J., Gill, C.O., Duff, P., Badoni, M. Saucier, L. (2008) Prevalence on beef carcasses of Mycobacterium avium ssp. paratuberculosis DNA. Int J Food Microbiol 124, 291 294.
53. Muehlherr, J.E., Zweifel, C., Corti, S., Blanco, J.E. Stephan, R. (2003) Microbiological quality of raw goat's and ewe's bulk-tank milk in Switzerland. J Dairy Sci 86, 3849 3856.
54. Muskens, J., Barkema, H.W., Russchen, E., van Maanen, K., Schukken, Y.H. Bakker, D. (2000) Prevalence and regional distribution of paratuberculosis in dairy herds in The Netherlands. Vet Microbiol 77, 253 261.
55. Nauta, M.J. Van der Giessen, J.W.Bvd. (1998) Human exposure to Mycobacterium avium paratuberculosis via pasteurised milk: a modelling approach. Vet Rec 143, 293 296.
56. Nielsen, S.S. Toft, N. (2009) A review of prevalences of paratuberculosis in farmed animals in Europe. Prev Vet Med 88, 1 14.
57. Nielsen, S.S., Grohn, Y.T., Quaas, R.L. Agger, J.F. (2002) Paratuberculosis in dairy cattle: variation of the antibody response in offspring attributable to the dam. J Dairy Sci 85, 406 412.
58. O'Reilly, C.E., O'Connor, L., Anderson, W., Harvey, P., Grant, I.R., Donaghy, J., Rowe, M. O'Mahony, P. (2004) Surveillance of bulk raw and commercially pasteurized cows' milk from approved Irish liquid-milk pasteurization plants to determine the incidence of Mycobacterium paratuberculosis. Appl Environ Microbiol 70, 5138 5144.
59. Obasanjo, I., Gröhn, Y.T. Mohammed, H.O. (1997) Farm factors associated with the presence of Mycobacterium paratuberculosis infection in dairy herds on the New York State paratuberculosis control program. Prev Vet Med 32, 243 251.
60. Pearce, L.E., Truong, H.T., Crawford, R.A., Yates, G.F., Cavaignac, S. de Lisle, G.W. (2001) Effect of turbulent-flow pasteurization on survival of Mycobacterium avium ssp. paratuberculosis added to raw milk. Appl Environ Microbiol 67, 3964 3969.
61. Rademaker, J.L., Vissers, M.M. Te Giffel, M.C. (2007) Effective Heat Inactivation of Mycobacterium avium ssp. paratuberculosis in raw milk contaminated with naturally infected faeces. Appl Environ Microbiol 73, 4185 4190.
62. Rossiter, C.A. Henning, W.R. (2001) Isolation of Mycobacterium paratuberculosis from thin market cows at slaughter. J Dairy Sci 84 (Suppl. 113.
63. Roussel, A.J., Libal, M.C., Whitlock, R.L., Hairgrove, T.B., Barling, K.S. Thompson, J.A. (2005) Prevalence of and risk factors for paratuberculosis in purebred beef cattle. J Am Vet Med Assoc 226, 773 778.
64. Sargeant, J.M., Amezcua, M.D.R., Rajić, A. Waddell, L. (2005) A Guide to Conducting Systematic Reviews in Agri-Food Public Health. Available at: http://dsp-psd.pwgsc.gc.ca/Collection/HP5-9-2005E.pdf.
65. Sargeant, J.M., Rajic, A., Read, S. Ohlsson, A. (2006) The process of systematic review and its application in agri-food public-health: review. Prev Vet Med 75, 141 151.
66. Scott, H.M., Sorensen, O., Wu, J.T., Chow, E.Y., Manninen, K. Van Leeuwen, J.A. (2006) Seroprevalence of Mycobacterium avium ssp. paratuberculosis, Neospora caninum, Bovine leukemia virus, and Bovine viral diarrhea virus infection among dairy cattle and herds in Alberta and agroecological risk factors associated with seropositivity. Can Vet J 47, 981 991.
67. Scott, H.M., Sorensen, O., Wu, J.T., Chow, E.Y. Manninen, K. (2007) Seroprevalence of and agroecological risk factors for Mycobacterium avium spp. paratuberculosis and neospora caninum infection among adult beef cattle in cow-calf herds in Alberta, Canada. Can Vet J 48, 397 406.
68. Singh, S.V. Vihan, V.S. (2004) Detection of Mycobacterium avium ssp. paratuberculosis in goat milk. Small Ruminant Res 54, 231 235.
69. Small, A., Reid, C.A. Buncic, S. (2003) Conditions in lairages at abattoirs for ruminants in southwest England and in vitro survival of Escherichia coli O157, Salmonella Kedougou, and Campylobacter jejuni on lairage-related substrates. J Food Prot 66, 1570 1575.
70. Sofos, J.N., Kochevar, S.L., Bellinger, G.R., Buege, D.R., Hancock, D.D., Ingham, S.C., Morgan, J.B., Reagan, J.O. et al. (1999) Sources and extent of microbiological contamination of beef carcasses in seven United States slaughtering plants. J Food Prot 62, 140 145.
71. Spahr, U. Schafroth, K. (2001) Fate of Mycobacterium avium ssp. paratuberculosis in Swiss hard and semihard cheese manufactured from raw milk. Appl Environ Microbiol 67, 4199 4205.
72. Stabel, J.R. (1998) Symposium: biosecurity and disease, Johnes' disease: a hidden threat. J Dairy Sci 81, 283 288.
73. Stabel, J.R. (2001) On-farm batch pasteurisation destroys Mycobacterium paratuberculosis in waste milk. J Dairy Sci 84, 524 527.
74. Stabel, J.R. Lambertz, A. (2004) Efficacy of pasteurization conditions for the inactivation of Mycobacterium avium ssp. paratuberculosis in milk. J Food Prot 67, 2719 2726.
75. Stephan, R., Schumacher, S., Tasara, T. Grant, I.R. (2007) Prevalence of Mycobacterium avium ssp. paratuberculosis in Swiss raw milk cheeses collected at the retail level. J Dairy Sci 90, 3590 3595.
76. Sung, N. Collins, M.T. (2000) Effect of three factors in cheese production (pH, salt, and heat) on Mycobacterium avium ssp. paratuberculosis viability. Appl Environ Microbiol 66, 1334 1339.
77. Sweeney, R.W., Whitlock, R.H. Rosenberger, A.E. (1992) Mycobacterium paratuberculosis cultured from milk and supramammary lymph nodes of infected asymptomatic cows. J Clin Microbiol 30, 166 171.
78. Taylor, T.K., Wilks, C.R. McQueen, D.S. (1981) Isolation of Mycobacterium avium paratuberculosis from the milk of a cow with JD. Vet Rec 109, 532 533.
79. Thorne, J.G. Hardin, L.E. (1997) Estimated prevalence of paratuberculosis in Missouri, USA cattle. Prev Vet Med 31, 51 57.
80. Uzoigwe, J.C., Khaitsa, M.L. Gibbs, P.S. (2007) Epidemiological evidence for Mycobacterium avium spp. paratuberculosis as a cause of Crohn's disease; Review article. Epidemiol Infect 20, 1 12.
81. Van Leeuwen, J.A., Keefe, G.P., Tremblay, R., Power, C. Wichtel, J.J. (2001) Seroprevalence of infection with Mycobacterium avium ssp. paratuberculosis, bovine leukemia virus, and bovine viral diarrhea virus in maritime Canada dairy cattle. Can Vet J 42, 193 198.
82. Waddell, L., Rajić, A., Sargeant, J., Harris, J., Amezcua, R., Downey, L., Read, S. McEwen, S. (2008) The zoonotic potential of Mycobacterium avium spp. paratuberculosis: A systematic review. Can J Public Health 99 : Available at http://journal.cpha.ca/index.php/cjph/article/view/1613.
83. Wells, S.J. Wagner, B.A. (2000) Herd-level risk factors for infection with Mycobacterium paratuberculosis in United States dairies and association between familiarity of the herd manager with the disease or prior diagnosis of the disease in that herd and use of preventive measures. J Am Vet Med Assoc 216, 1450 1457.
84. Whitlock, R.H. Buergelt, C. (1996) Preclinical and clinical manifestations of paratuberculosis (including pathology). Vet Clin N Am Food Anim Pract 12, 345 356.