An inter-laboratory ring trial for the detection and isolation of Mycobacterium avium subsp. paratuberculosis from raw milk artificially contaminated with naturally infected faeces

Food Microbiology

Volumn 25, Issue 1, 2008, Pages 128-135

  Donaghy, J A ^a   Rowe, M T ^a,b   Rademaker, J L W ^c   Hammer, P ^d   Herman, L ^e   De Jonghe, V ^e   Blanchard, B ^f   Duhem, K ^g   Vindel, E ^g  

^a AGRI FOOD AND BIOSCIENCES INSTITUTE   (United Kingdom)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c NIZO FOOD RESEARCH   (Netherlands)

^d FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

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

^f ADIAGENE   (France)

^g CNIEL   (France)

Author keywords

Milk; Mycobacterium avium subsp. paratuberculosis; PCR detection

Indexed keywords

BACTERIAL DNA;

ANALYTICAL EQUIPMENT; ANIMAL; ARTICLE; BACTERIAL COUNT; CATTLE; DIAGNOSIS, MEASUREMENT AND ANALYSIS; FECES; FOOD CONTAMINATION; GENE AMPLIFICATION; HUMAN; ISOLATION AND PURIFICATION; METHODOLOGY; MICROBIOLOGY; MILK; MYCOBACTERIUM AVIUM; POLYMERASE CHAIN REACTION; REPRODUCIBILITY; SAFETY; SENSITIVITY AND SPECIFICITY; STANDARD;

ANIMALS; CATTLE; COLONY COUNT, MICROBIAL; CONSUMER PRODUCT SAFETY; DNA, BACTERIAL; FECES; FOOD CONTAMINATION; GENE AMPLIFICATION; HUMANS; LABORATORY TECHNIQUES AND PROCEDURES; MILK; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; POLYMERASE CHAIN REACTION; REAGENT KITS, DIAGNOSTIC; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

CORYNEBACTERINEAE; MYCOBACTERIUM; MYCOBACTERIUM AVIUM; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS;

EID: 35948955927     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2007.06.007     Document Type: Article

References (60)

1. Abubakar I., Myhill D.J., Hart A.R., Lake I., Harvey I., Rhodes J.M., Robinson R., Lobo A.J., Probert C.S.J., and Hunter P.R. A case-control study of drinking water and dairy products in Crohn's disease-further investigation of the possible role of Mycobacterium avium paratuberculosis. Am J Epidemiol. 19 (2007) 2007 Advance Access published on January 19, 2007. doi:10.1093/aje/kwk067
2. Ayele W.Y., Svastova P., Roubal P., Bartos M., and Pavlik I. Mycobacterium avium subsp. paratuberculosis cultured from locally and commercially pasteurized cow's milk in the Czech Republic. Appl. Environ. Microbiol. 71 (2005) 1014-1210
3. Beard P.M., Daniels M.J., Henderson D., Pirie A., Rudge K., Buxton D., Rhind S., Greig A., Hutchings M.R., McKendrick I., Stevenson K., and Sharp J.M. Paratuberculosis infection of nonruminant wildlife in Scotland. J. Clin. Microbiol. 39 (2001) 1517-1521
4. Breed R.S. The determination of the number of bacteria in milk by direct microscopic examination. Centralb. F. Bakt. 30 (1911) 337-340
5. Christopher-Hennings J., Dammen M.A., Weeks S.R., Epperson W.B., Singh S.N., Steinlicht G.L., Fang Y., Skaare J.L., Larsen J.L., Payeur J.B., and Nelson E.A. Comparison of two DNA extractions and nested PCR, real-time PCR, a new commercial PCR assay and bacterial culture for detection of Mycobacterium avium subsp. paratuberculosis in bovine feces. J. Vet. Diagn. Invest. 15 (2003) 87-93
6. Clark D.L., Anderson J.L., Koziczkowski J.J., and Ellingson J.L.E. Detection of Mycobacterium avium subsp. paratuberculosis genetic components in retail cheese curds purchased in Wisconsin and Minnesota by PCR. Mol. Cell. Probes 20 (2006) 197-202
7. Cocito C., Gilot P., Coene M., De Kesel M., Poupart P., and Vanuffel P. Paratuberculosis. Clin. Microbiol. Rev. 7 (1994) 328-345
8. Collins M.T. Paratuberculosis: review of present knowledge. Acta Vet. Scand. 44 (2003) 217-221
9. Collins M.T. Update on paratuberculosis: 3. Control and zoonotic potential. Ir. Vet. J. 57 (2004) 49-52
10. Corti S., and Stephan R. Detection of Mycobactrium avium subsp. paratuberculosis specific IS900 insertion sequences in bulk-tank milk samples obtained from different regions throughout Switzerland. BMC Microbiol. 2 (2002) 15
11. Djonne B., Jensen M.R., Grant I.R., and Holstad G. Detection by immunomagnetic PCR of Mycobacterium avium subsp. paratuberculosis in milk from dairy goats in Norway. Vet. Microbiol. 92 (2003) 135-143
12. Ellingson J., Anderson J.L.K., Koziczkowski J.J., Radcliff R.P., Sloan S.J., Allen S.E., and Sullivan N.M. Detection of viable Mycobacterium avium subsp. paratuberculosis in retail pasteurised whole milk by two culture methods and PCR. J. Food Prot. 68 (2005) 966-972
13. Englund S., Ballagi-Pordany A., Bolske G., and Johansson K.E. Single PCR and nested PCR with a mimic molecule for detection of Mycobacterium avium subsp. paratuberculosis. Diagn. Microbiol. Infect. Dis. 33 3 (1999) 163-171
14. Fang Y., Wu W.H., Pepper J.L., Larsen J.L., Marras S.A., Nelson E.A., Epperson W.B., and Christopher-Hennings J. Comparison of real-time, quantitative PCR with molecular beacons to nested PCR and culture methods for detection of Mycobacterium avium subsp. paratuberculosis in bovine faecal samples. J. Clin. Microbiol. 40 (2002) 287-291
15. Gao A., Mutharia L., Chen S., Rahn K., and Odumeru J. Effect of pasteurisation on survival of Mycobacterium paratuberculosis in milk. J. Dairy Sci. 85 (2002) 3198-3205
16. Giese S.B., and Ahrens P. Detection of Mycobacterium avium subsp. paratuberculosis in milk form clinically affected cows by PCR and culture. Vet. Microbiol. 77 (2000) 291-297
17. Grant I.R. Mycobacterium avium ssp. paratuberculosis in foods: current evidence and potential consequences. Int. J. Dairy Tech. 59 (2006) 112-117
18. Grant I.R., and Rowe M.T. Methods for the detection and enumeration of viable Mycobacterium paratuberculosis from milk and milk products. Bull. Int. Dairy Fed. 362 (2001) 41-52
19. Grant I.R., Ball H.J., Neill S.D., and Rowe M.T. Inactivation of Mycobacterium paratuberculosis in cow's milk at pasteurisation temperatures. Appl. Environ. Microbiol. 62 (1996) 631-636
20. Grant I.R., Ball H.J., and Rowe M.T. Isolation of Mycobacterium paratuberculosis from milk by immunomagnetic separation. Appl. Environ. Microbiol. 64 (1998) 3153-3158
21. Grant I.R., Ball H.J., and Rowe M.T. Effect of high temperature, short time pasteurisation on milk containing low numbers of Mycobacterium paratuberculosis. Lett. Appl. Microbiol. 26 (1998) 166-170
22. Grant I.R., Pope C.M., O'Riordan L.M., Ball H.J., and Rowe M.T. Improved detection of Mycobacterium avium subsp. paratuberculosis in milk by immunomagnetic PCR. Vet. Microbiol. 77 (2000) 369-378
23. Grant I.R., Ball H.J., and Rowe M.T. Incidence of Mycobacterium avium subsp. paratuberculosis in bulk raw and commercially pasteurised cow's milk from approved dairy processing establishments in the United Kingdom. Appl. Environ. Microbiol. 68 (2002) 2428-2435
24. Grant I.R., Kirk R.B., Hitchings E., and Rowe M.T. Comparative evaluation of the MGIT and BACTEC culture systems for the recovery of Mycobacterium avium subsp. paratuberculosis from milk. J. Appl. Microbiol. 95 (2003) 196-201
25. Grant I.R., Williams A.G., Rowe M.T., and Muir D.D. Efficacy of various pasteurisation time/temperature conditions in combination with homogenisation on the inactivation of Mycobacterium avium subsp. paratuberculosis in milk. Appl. Environ. Microbiol. 71 (2005) 2853-2861
26. Greig A., Stevenson K., Henderson D., Perez V., Hughes V., Pavlik I., Hines M.E., McKendrick I., and Sharp J.M. Epidemiological study of paratuberculosis in wild rabbits in Scotland. J. Clin. Microbiol. 37 (1999) 1746-1751
27. Hammer P., Kiesner C., Walte H.G., Knappstein K., and Teufel P. Heat resistance of Mycobacterium avium subsp. paratuberculosis in raw milk tested in a pilot plant pasteuriser. Kiel. Milchwirtschaftliche Forsch. 54 (2002) 275-303
28. Herman L.M.F., De Block J.G.E., and Moermans R.J.B. Direct detection of Listeria monocytogenes in 25 ml of raw milk by a two-step PCR with nested primers. Appl. Environ. Microbiol. 61 (1995) 817-819
29. Herthnek D., Englund S., Willemsen P.T.J., and Bolske G. Sensitive detection of Mycobacterium avium subsp. paratuberculosis in bovine semen by real-time PCR. J. Appl. Microbiol. 100 (2006) 1095-1102
30. Hope, A.F., Tulk, P.A., Condron, R.J., 1996. Pasteurisation of Mycobacterium paratuberculosis in whole milk. In: Proceedings of the Fifth International Colloqium on Paratuberculosis, pp. 377-382.
31. Kim S.G., Kim E.H., Lafferty C.J., Miller L.J., Koo H.J., Stehman S.M., and Shin S.J. Use of conventional and real-time polymerase chain reaction for confirmation of Mycobacterium avium subsp. paratuberculosis in a broth-based culture system ESP II. J. Vet. Diagn. Invest. 16 (2004) 448-453
32. Mc Donald W.L., O'Riley K., Schroen C.J., and Condron R.J. Heat inactivation of Mycobacterium avium subsp. paratuberculosis in milk. Appl. Environ. Microbiol. 71 (2005) 1785-1789
33. Microbial Safety of Food Funders Group, 2006. Report on the UK Publicly Funded Research Relating to Mycobacterium avium subsp. paratuberculosis. [Internet document] URL 〈www.food.gov.uk/science/research/researchinfo/foodborneillness/mic rofunders/msffgmapreport〉.
34. Millar D., Ford J., Sanderson J., Withey S., Tizard M., Doran T., and Hermon-Taylor J. IS900 PCR to detect Mycobacterium paratuberculosis in retail supplies of whole pasteurised cows' milk in England and Wales. Appl. Environ. Microbiol. 62 (1996) 3446-3452
35. Moss M.T., Sanderson J.D., Tizard M.L., Hermon-Taylor J., El Zaatari F.A., Markesich D.C., and Graham D.Y. Polymerase chain reaction detection of Mycobacterium paratuberculosis and Mycobacterium avium subsp. silvaticum in long term cultures from Crohn's disease and control tissues. Gut 33 (1992) 1209-1213
36. Nielsen S.S., Nielsen K.K., Huda A., Condron R., and Collins M.T. Diagnostic techniques for paratuberculosis. Bull. Int. Dairy Fed. 362 (2001) 5-17
37. O'Mahony J., and Hill C. A real-time PCR assay for the detection and quantitation of Mycobacterium avium subsp. paratuberculosis using SYBR Green and the light cycler. J. Microbiol. Methods 51 (2002) 283-293
38. O'Mahony J., and Hill C. Rapid real-time PCR for detection and quantitation of Mycobacterium avium subsp. paratuberculosis DNA in artificially contaminated milk. Appl. Environ. Microbiol. 70 (2004) 4561-4568
39. O'Reilly C.E., O'Connor L., Anderson W., Harvey P., Grant I.R., Donaghy J., Rowe M., and O'Mahony P. Surveillance of bulk raw and commercially pasteurised cow's milk from approved Irish liquid-milk pasteurisation plants to determine the incidence of Mycobacterium paratuberculosis. Appl. Environ. Microbiol. 70 (2004) 5138-5144
40. Odumeru J., Gao A., Chen S., Raymond M., and Mutharia L. Use of the bead beater for preparation of Mycobacterium paratuberculosis template DNA in milk. Can. J. Vet. Res. 65 (2001) 201-205
41. Pearce L.E., Truong H.T., Crawford R.A., Yates G.F., Cavaignac S., and De Lisle G.W. Effect of turbulent-flow pasteurization on survival of Mycobacterium avium subspecies paratuberculosis added to raw milk. Appl. Environ. Microbiol. 67 (2001) 3964-3969
42. Pillai S.R., and Jayarao B.M. Application of IS900 PCR for detection of Mycobacterium avium subsp. paratuberculosis directly from raw milk. J. Dairy Sci. 85 (2002) 1052-1057
43. Rademaker, J.L.W., Meeuwisse, J., te Giffel, M.C., 2003. Heat inactivation of Mycobacterium avium subspecies paratuberculosis. In: Juste, R.A., Geijo, M.V., Garrido J.M. (Eds.), Proceedings of the Seventh International Colloqium on Paratuberculosis, Bilbao, Spain. The International Association for Paratuberculosis, Inc., Madison, WI, USA, pp. 317-319.
44. Rademaker J.L.W., Vissers M.M.M., and te Giffel M.C. Heat inactivation of Mycobacterium avium subspecies paratuberculosis in raw milk inoculated with cow-feces using a pilot scale turbulent flow pasteurizer. Appl. Environ. Microbiol. 73 (2007) 4185-4190
45. Rodriguez-Lazaro D., D'Agostino M., Herrewegh A., Pla M., Cook N., and Ikonomopoulos J. Real-time PCR-based methods for the detection of Mycobacterium avium subsp. paratuberculosis in water and milk. Int. J. Food Micro. 101 (2005) 93-104
46. Stabel J.R., and Lambertz A. Efficacy of pasteurization conditions for the inactivation of Mycobacterium avium subsp. paratuberculosis in milk. J. Food Prot. 67 (2004) 2719-2726
47. Stabel J.R., Steadham E.M., and Bolin C.A. Heat inactivation of Mycobacterium paratuberculosis in raw milk: are current pasteurization conditions effective?. Appl. Environ. Microbiol. 63 (1997) 4975-4977
48. Stabel J.R., Wells S.J., and Wagner B.A. Relationships between fecal culture, ELISA and bulk tank milk results for Johne's disease in US dairy herds. J. Dairy Sci. 85 (2002) 525-531
49. Stabel J.R., Bosworth T.L., Kirkbride T.A., Forde R.L., and Whitlock R.H. A simple, rapid and effective method for the extraction of Mycobacterium paratuberculosis DNA from fecal samples for polymerase chain reaction. J. Vet. Diagn. Invest. 16 (2004) 22-30
50. Stephan R., Buhler K., and Corti S. Incidence of Mycobacterium avium subsp. paratuberculosis in bulk-tank milk samples from different regions of Switzerland. Vet. Rec. 150 (2002) 214-215
51. Stich R.W., Byrum B., Love B., Theus N., Barber L., and Shulaw W.P. Evaluation of an automated system for non-radiometric detection of Mycobacterium avium subsp. paratuberculosis in bovine faeces. J. Microbiol. Methods 56 (2004) 267-275
52. Stratmann J., Strommenger B., Stevenson K., and Gerlach G.F. Development of a peptide-mediated capture PCR for detection of Mycobacterium avium subspecies paratuberculosis in milk. J. Clin. Microbiol. 40 (2002) 4244-4250
53. Sung N., and Collins M.T. Thermal tolerance of Mycobacterium paratuberculosis. Appl. Environ. Microbiol. 64 (1998) 999-1005
54. Taddei S., Robbi C., Cesena C., Rossi I., Schiano E., Arrigoni N., Vicenzoni G., and Cavirani S. Detection of Mycobacterium avium subsp. paratuberculosis in bovine faecal samples: comparison of three polymerase chain reaction-based diagnostic tests with a conventional culture method. J. Vet. Diagn. Invest. 16 (2004) 503-508
55. Tasara T., and Stephan R. Development of an F57 sequence-based real-time PCR assay for detection of Mycobacterium avium subsp. paratuberculosis in milk. Appl. Environ. Microbiol. 71 (2005) 5957-5968
56. Tasara T., Hoelzle L.E., and Stephan R. Development and evaluation of a Mycobacterium avium subspecies paratuberculosis (Map) specific multiplex PCR assay. Int. J. Food Microbiol. 104 (2005) 279-287
57. Vansnick E., De Rijk P., Vercammen F., Geysen D., Rigouts L., and Portaels F. Newly developed primers for the detection of Mycobacterium avium subsp. paratuberculosis. Vet. Microbiol. 100 (2004) 197-204
58. Vary P.H., Andersen P.R., Green E., Hermon-Taylor J., and McFadden J.J. Use of highly specific DNA probes and the polymerase chain reaction to detect Mycobacterium paratuberculosis in Johne's disease. J. Clin. Microbiol. 28 (1990) 933-937
59. Whan L., Ball H.J., Grant I.R., and Rowe M.T. Development of an IMS-PCR assay for the detection of Mycobacterium avium subsp. paratuberculosis in water. Lett. Appl. Microbiol. 40 (2005) 269-273
60. Whittington R.J., Marsh I., Turner M.J., McAllister S., Choy E., Eamens G.J., Marshall D.J., and Ottaway S. Rapid detection of Mycobacterium paratuberculosis in clinical samples from ruminants and in spiked environmental samples by modified BACTEC 12B radiometric culture and direct confirmation by IS900 PCR. J. Clin. Microbiol. 36 (1998) 701-707