Occurrence of Mycobacterium avium subsp. paratuberculosis in milk at dairy cattle farms: A systematic review and meta-analysis

Veterinary Microbiology

Volumn 157, Issue 3-4, 2012, Pages 253-263

  Okura, Hisako ^a   Toft, Nils ^a   Nielsen, Søren Saxmose ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Meta analysis; Milk; Paratuberculosis; Prevalence; Systematic review

Indexed keywords

BACTERIAL LOAD; BACTERIUM CULTURE; CATTLE FARMING; DAIRY CATTLE; ENZYME LINKED IMMUNOSORBENT ASSAY; HERD; META ANALYSIS; MILK; MYCOBACTERIUM PARATUBERCULOSIS; NONHUMAN; PASTEURIZATION; POLYMERASE CHAIN REACTION; REVIEW; SENSITIVITY AND SPECIFICITY; SYSTEMATIC REVIEW;

ANIMALS; CATTLE; CATTLE DISEASES; FEMALE; FOOD CONTAMINATION; FOOD MICROBIOLOGY; MILK; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; PARATUBERCULOSIS; PASTEURIZATION; POLYMERASE CHAIN REACTION; PREVALENCE;

BOS; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS;

EID: 84860533259     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2011.12.019     Document Type: Review

References (75)

1. Barrington G.M., Gay J.M., Eriks I.S., Davis W.C., Evermann J.F., Emerson C., O'Rourke J.L., Hamilton M.J., Bradway D.S. Temporal patterns of diagnostic results in serial samples from cattle with advanced paratuberculosis infections. J. Vet. Diagn. Invest. 2003, 15:195-200.
2. Borenstein M. Introduction to Meta-analysis 2009, Wiley-Blackwell, Chichester, United Kingdom.
3. Bosshard C., Stephan R., Tasara T. Application of an F57 sequence-based real-time PCR assay for Mycobacterium paratuberculosis detection in bulk tank raw milk and slaughtered healthy dairy cows. J. Food Prot. 2006, 69:1662-1667.
4. Botsaris G., Slana I., Liapi M., Dodd C., Economides C., Rees C., Pavlik I. Rapid detection methods for viable Mycobacterium avium subspecies paratuberculosis in milk and cheese. Int. J. Food Microbiol. 2010, 141(Suppl. 1):S87-S90.
5. Buergelt C.D., Williams J.E. Nested PCR on blood and milk for the detection of Mycobacterium avium subsp paratuberculosis DNA in clinical and subclinical bovine paratuberculosis. Aust. Vet. J. 2004, 82:497-503.
6. Caldow G., Strain S.A.J., Chapman Z., Kemp R., Cook A.J. A survey to estimate the herd level prevalence of paratuberculosis in the dairy herd of the United Kingdom. Cattle Pract. 2007, 15:169-171.
7. Carvalho I.A., Silva A., Campos V.E., Moreira M.A. Short communication: detection of Mycobacterium avium subspecies paratuberculosis by polymerase chain reaction in bovine milk in Brazil. J. Dairy Sci. 2009, 92:5408-5410.
8. Corti S., Stephan R. Detection of Mycobacterium avium subspecies paratuberculosis specific IS900 insertion sequences in bulk-tank milk samples obtained from different regions throughout Switzerland. BMC Microbiol. 2002, 2:15.
9. DimareliMalli Z. Detection of Mycobacterium avium subsp. paratuberculosis in milk from clinically affected sheep and goats. Int. J. Appl. Res. Vet. Med. 2010, 8:44-50.
10. Djønne B., Jensen M.R., Grant I.R., Holstad G. Detection by immunomagnetic PCR of Mycobacterium avium subsp. paratuberculosis in milk from dairy goats in Norway. Vet. Microbiol. 2003, 92:135-143.
11. Dohoo I., Martin W., Stryhn H. Veterinary Epidemiologic Research 2009, VER Inc., Charlottetown, Canada, pp. 739-772.
12. Dzieciol M., Volgger P., Khol J., Baumgartner W., Wagner M., Hein I. A novel real-time PCR assay for specific detection and quantification of Mycobacterium avium subsp, paratuberculosis in milk with the inherent possibility of differentiation between viable and dead cells. BMC Res. Notes 2010, 3:251.
13. Eltholth M.M., Marsh V.R., Van Winden S., Guitian F.J. contamination of food products with Mycobacterium avium paratuberculosis: a systematic review. J. Appl. Microbiol. 2009, 107:1061-1071.
14. Favila-Humara L.C., Chavez-Gris G.G., Carrillo-Casas E.M., Hernandez-Castro R. Mycobacterium avium subsp. paratuberculosis detection in individual and bulk tank milk samples from bovine herds and caprine flocks. Foodborne Pathog. Dis. 2010, 7:351-355.
15. Gao A., Odumeru J., Raymond M., Hendrick S., Duffield T., Mutharia L. Comparison of milk culture, direct and nested polymerase chain reaction (PCR) with fecal culture based on samples from dairy herds infected with Mycobacterium avium subsp. paratuberculosis. Can. J. Vet. Res. 2009, 73:58-64.
16. Gardner I.A. An epidemiologic critique of current microbial risk assessment practices: the importance of prevalence and test accuracy data. J. Food Prot. 2004, 67:2000-2007.
17. Gardner I.A., Nielsen S.S., Whittington R.J., Collins M.T., Bakker D., Harris B., Sreevatsan S., Lombard J.E., Sweeney R., Smith D.R., Gavalchin J., Eda S. Consensus-based reporting standards for diagnostic test accuracy studies for paratuberculosis in ruminants. Prev. Vet. Med. 2011, 101:18-34.
18. Giese S.B., Ahrens P. Detection of Mycobacterium avium subsp. paratuberculosis in milk from clinically affected cows by PCR and culture. Vet. Microbiol. 2000, 77:291-297.
19. Grant I.R., Hitchings E.I., McCartney A., Ferguson F., Rowe M.T. Effect of commercial-scale high-temperature, short-time pasteurization on the viability of Mycobacterium paratuberculosis in naturally infected cows' milk. Appl. Environ. Microbiol. 2002, 68:602-607.
20. Grant I.R., Pope C.M., O'Riordan L.M., Ball H.J., Rowe M.T. Improved detection of Mycobacterium avium subsp. paratuberculosis in milk by immunomagnetic PCR. Vet. Microbiol. 2000, 77:369-378.
21. Grant I.R., Williams A.G., Rowe M.T., Muir D.D. Efficacy of various pasteurization time-temperature conditions in combination with homogenization on inactivation of Mycobacterium avium subsp. paratuberculosis in milk. Appl. Environ. Microbiol. 2005, 71:2853-2861.
22. Haghkhah M., Ansari-Lari M., Novin-Baheran A.M., Bahramy A. Herd-level prevalence of Mycobacterium avium subspecies paratuberculosis by bulk-tank milk PCR in Fars province (Southern Iran) Dairy Herds. Prev. Vet. Med. 2008, 86:8-13.
23. Hasonova L., Trcka I., Babak V., Rozsypalova Z., Pribylova R., Pavlik I. Distribution of Mycobacterium avium subsp. paratuberculosis in tissues of naturally infected cattle as affected by age. Vet. Med. 2009, 54:257-269.
24. Hermon-Taylor J., Cheng J., Bull T. Mycobacterium avium subsp. paratuberculosis in milk: an animal and human pathogen (meeting abstract). J. Microbiol. Methods 1999, 38:217.
25. Herthnek D., Nielsen S.S., Lindberg A., Bolske G. A robust method for bacterial lysis and DNA purification to be used with real-time PCR for detection of Mycobacterium avium subsp. paratuberculosis in milk. J. Microbiol. Methods 2008, 75:335-340.
26. Higgins, J.P., Green, S., 2011. Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration. Available at: http://www.cochrane.org/training/cochrane-handbook.
27. Higgins J.P., Thompson S.G. Quantifying heterogeneity in a meta-analysis. Stat. Med. 2002, 21:1539-1558.
28. Ikonomopoulos J., Liandris E., Andreadou M., Gazouli M. Associations between abortion-records in goats and test-positivity to Mycobacterium avium subsp. paratuberculosis. Open Vet. Sci. J. 2009, 3:1-5.
29. Jayarao B.M., Pillai S.R., Wolfgang D.R., Griswold D.R., Rossiter C.A., Tewari D., Burns C.M., Hutchinson L.J. Evaluation of IS900-PCR assay for detection of Mycobacterium avium subspecies paratuberculosis infection in cattle using quarter milk and bulk tank milk samples. Foodborne Pathog. Dis. 2004, 1:17-26.
30. Kaittanis C., Naser S.A., Perez J.M. One-step, nanoparticle-mediated bacterial detection with magnetic relaxation. Nano Lett. 2007, 7:380-383.
31. Kaur P., Filia G., Singh S.V., Patil P.K., Sandhu K.S. Molecular detection and typing of Mycobacterium avium subspecies paratuberculosis from milk samples of dairy animals. Trop. Anim. Health Prod. 2010, 42:1031-1035.
32. Konuk M., Korcan E., Dulgerbaki S., Altindis M. Isolation and identification of Mycobacteria from raw milk samples in Afyonkarahisar District of Turkey. Int. J. Food Microbiol. 2007, 115:343-347.
33. Kudahl A.B., Sorensen J.T., Nielsen S.S., Ostergaard S. Simulated economic effects of improving the sensitivity of a diagnostic test in paratuberculosis control. Prev. Vet. Med. 2007, 78:118-129.
34. Kumar S., Singh S.V., Sevilla I., Singh A.V., Whittington R.J., Juste R.A., Sharma G., Singh P.K., Sohal J.S. Lacto-prevalence, genotyping of Mycobacterium avium subspecies paratuberculosis and evaluation of three diagnostic tests in milk of naturally infected goatherds. Small Ruminant Res. 2008, 74:37-44.
35. Metzger-Boddien C., Khaschabi D., Schonbauer M., Boddien S., Schlederer T., Kehle J. Automated high-throughput immunomagnetic separation-PCR for detection of Mycobacterium avium subsp. paratuberculosis in bovine milk. Int. J. Food Microbiol. 2006, 110:201-208.
36. Muehlherr J.E., Zweifel C., Corti S., Blanco J.E., Stephan R. Microbiological quality of raw goat's and ewe's bulk-tank milk in Switzerland. J. Dairy Sci. 2003, 86:3849-3856.
37. Nebbia P., Robino P., Zoppi S., De Meneghi D. Detection and excretion pattern of Mycobacterium avium subspecies paratuberculosis in milk of asymptomatic sheep and goats by nested-PCR. Small Ruminant Res. 2006, 66:116-120.
38. O'Reilly C.E., O'Connor L., Anderson W., Harvey P., Grant I.R., Donaghy J., Rowe M., O'Mahony P. 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. 2004, 70:5138-5144.
39. Paolicchi F.A., Zumarraga M.J., Gioffre A., Zamorano P., Morsella C., Verna A., Cataldi A., Alito A., Romano M. Application of different methods for the diagnosis of paratuberculosis in a dairy cattle herd in Argentina. J. Vet. Med. B: Infect. Dis. Vet. Public Health 2003, 50:20-26.
40. Pillai S.R., Jayarao B.M. Application of IS900 PCR for detection of Mycobacterium avium subsp. paratuberculosis directly from raw milk. J. Dairy Sci. 2002, 85:1052-1057.
41. Pinedo P.J., Rae D.O., Williams J.E., Donovan G.A., Melendez P., Buergelt C.D. Association among results of serum ELISA, faecal culture and nested PCR on milk, blood and faeces for the detection of paratuberculosis in dairy cows. Transbound Emerg. Dis. 2008, 55:125-133.
42. Pinedo P.J., Williams J.E., Monif G.R.G., Rae D.O., Buergelt C.D. Mycobacterium paratuberculosis shedding into milk: association of ELISA seroreactivity with DNA detection in milk. Int. J. Appl. Res. Vet. Med. 2008, 6:137-144.
43. R Development Core Team, 2010. R: A Language and Environment for Statistical Computing.
44. Rademaker J.L., Vissers M.M., Te Giffel M.C. Effective heat inactivation of Mycobacterium avium subsp. paratuberculosis in raw milk contaminated with naturally infected feces. Appl. Environ. Microbiol. 2007, 73:4185-4190.
45. Ridge S.E., Andreata S., Jones K., Cantlon K., Francis B., Florisson N., Gwozdz J. Inter-laboratory comparison of radiometric culture for Mycobacterium avium subsp. paratuberculosis using raw milk from known infected herds and individual dairy cattle in Victoria. Aust. Vet. J. 2010, 88:249-254.
46. Ronald B.S.M., Narayanan R., Krishnakumar N., Baegan S., Manohar B.M. Detection of Mycobacterium avium subsp. paratuberculosis excretion in goat milk. Asian J. Microbiol. Biotechnol. Environ. Sci. 2009, 11:457-460.
47. Sargeant J.M., Amezcua M.D.R., Rajic A., Waddell L. A Guide to Conducting Systematic Reviews in Agri-Food Public Health 2005, Food Safety Research and Response Network.
48. Selvam A., Vijayarani K., Kumanan K. Detection of Mycobacterium avium subsp paratuberculosis in milk of asymptomatic sheep by polymerase chain reaction. Indian J. Anim. Sci. 2009, 79:784-785.
49. Seyyedin M., Salehi T.Z., Tadjbakhsh H., Najafi M.F., Rabbani M. Isolation and identification of Mycobacterium avium subsp. paratuberculosis from milk, manure and fecal samples of holstein-friesian dairy cattle. Pakistan J. Biol. Sci. 2008, 11:2639-2645.
50. Seyyedin M., Zahraei T., Najafi M.F. Comparison of isolation frequency of Mycobacterium avium subspecies paratuberculosis from different types of samples. Pakistan Vet. J. 2010, 30:143-149.
51. Shankar H., Singh S.V., Singh P.K., Singh A.V., Sohal J.S., Greenstein R.J. Presence, characterization, and genotype profiles of Mycobacterium avium subspecies paratuberculosis from unpasteurized individual and pooled milk, commercial pasteurized milk, and milk products in India by culture, PCR, and PCR-REA methods. Int. J. Infect. Dis. 2010, 14:e121-e126.
52. Sharma G., Singh S.V., Sevilla I., Singh A.V., Whittington R.J., Juste R.A., Kumar S., Gupta V.K., Singh P.K., Sohal J.S., Vihan V.S. Evaluation of indigenous milk ELISA with m-Culture and m-PCR for the diagnosis of bovine Johne's disease (BJD) in lactating Indian dairy cattle. Res. Vet. Sci. 2008, 84:30-37.
53. Singh S.V., Vihan V.S. Detection of Mycobacterium avium subspecies paratuberculosis in goat milk. Small Ruminant Res. 2004, 54:231-235.
54. Singh S.V., Singh A.V., Singh R., Sandhu K.S., Singh P.K., Sohal J.S., Gupta V.K., Vihan V.S. Evaluation of highly sensitive indigenous milk ELISA Kit with fecal culture, milk culture and fecal-PCR for the diagnosis of bovine Johne's disease (BJD) in India. Comp. Immunol. Microbiol. Infect. Dis. 2007, 30:175-186.
55. Singh S.V., Singh A.V., Singh R., Sandhu K.S., Singh P.K., Sohal J.S. Comparison of multiple diagnostic tests for the diagnosis of bovine paratuberculosis in lactating cows. Indian J. Anim. Sci. 2007, 77:1115-1117.
56. Singh S.V., Singh P.K., Singh A.V., Sohal J.S., Subodh S., Narayanasamy K. Non-chemical method of DNA recovery and characterization of Mycobacterium avium subspecies paratuberculosis using IS900 PCR. Indian J. Exp. Biol. 2007, 45:812-816.
57. Slana I., Kralik P., Kralova A., Pavlik I. On-farm spread of Mycobacterium avium subsp. paratuberculosis in raw milk studied by IS900 and F57 competitive real time quantitative PCR and culture examination. Int. J. Food Microbiol. 2008, 128:250-257.
58. Slana I., Bartos M., Roubal P., Babak V., Pavlik I. Mycobacterium avium subsp. paratuberculosis and M. a. avium detected by culture, IS900 and IS901 highly sensitive PCR in Bulk tank milk from dairy herds in the Czech Republic between 2002 and 2004. Czech J. Food Sci. 2009, 27:372-378.
59. Slana I., Liapi M., Moravkova M., Kralova A., Pavlik I. Mycobacterium avium subsp. paratuberculosis in cow bulk tank milk in Cyprus detected by culture and quantitative IS900 and F57 real-time PCR. Prev. Vet. Med. 2009, 89:223-226.
60. Smith W.L., McGarvey K.L., Cullor J.S. The use of spiral plating and microscopic colony counting for the rapid quantitation of Mycobacterium paratuberculosis. Lett. Appl. Microbiol. 2003, 36:293-296.
61. Soltani M., Nassiry M.R., Shahroudi F.E., Bassam M.R. Detection of Mycobacterium paratuberculosis in feces and milk samples from holstein dairy cows by PCR. Biotechnology 2008, 7:582-585.
62. Stabel J.R., Wells S.J., Wagner B.A. Relationships between fecal culture, ELISA, and bulk tank milk test results for Johne's disease in US dairy herds. J. Dairy Sci. 2002, 85:525-531.
63. Stephan R., Buhler K., Corti S. Incidence of Mycobacterium avium subspecies paratuberculosis in bulk-tank milk samples from different regions in Switzerland. Vet. Rec. 2002, 150:214-215.
64. Stratmann J., Dohmann K., Heinzmann J., Gerlach G.F. Peptide aMptD-mediated capture PCR for detection of Mycobacterium avium subsp. paratuberculosis in bulk milk samples. Appl. Environ. Microbiol. 2006, 72:5150-5158.
65. Stratmann J., Strommenger B., Stevenson K., Gerlach G.F. Development of a peptide-mediated capture PCR for detection of Mycobacterium avium subsp. paratuberculosis in milk. J. Clin. Microbiol. 2002, 40:4244-4250.
66. Streeter R.N., Hoffsis G.F., Bech-Nielsen S., Shulaw W.P., Rings D.M. Isolation of Mycobacterium paratuberculosis from colostrum and milk of subclinically infected cows. Am. J. Vet. Res. 1995, 56:1322-1324.
67. Szteyn J., Wiszniewska-Laszczych A., Ruszczynska A. Effectiveness of Mycobacterium paratuberculosis isolation from raw milk by means of direct isolation of DNA and classic culture. Pol. J. Vet. Sci. 2008, 11:25-28.
68. Taddei R., Barbieri I., Pacciarini M.L., Fallacara F., Belletti G.L., Arrigoni N. Mycobacterium porcinum strains isolated from bovine bulk milk: implications for Mycobacterium avium subsp. paratuberculosis detection by PCR and culture. Vet. Microbiol. 2008, 130:338-347.
69. Tasara T., Stephan R. Development of an F57 sequence-based real-time PCR assay for detection of Mycobacterium avium subsp. paratuberculosis in milk. Appl. Environ. Microbiol. 2005, 71:5957-5968.
70. Viechtbauer W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 2010, 36:1.
71. von Elm E., Altman D.G., Egger M., Pocock S.J., Gotzsche P.C., Vandenbroucke J.P. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 2007, 370:1453-1457. STROBE Initiative.
72. Wells S.J. Is milk or feces more important in transmission of map?. Proceedings of the North American Veterinary Conference, Large Animal, vol. 19 2005, 55.
73. Whittington R.J., Sergeant E.S. Progress Towards understanding the spread, detection and control of Mycobacterium avium subsp paratuberculosis in animal populations. Aust. Vet. J. 2001, 79:267-278.
74. Wilson D.J., Rood K., Biswas P., Byrem T.M. Herd-level prevalence of Johne's disease in Utah and adjacent areas of the intermountain West as detected by a bulk-tank milk surveillance project. J. Dairy Sci. 2010, 93:5792-5797.
75. Wiszniewska-Laszczych A., Szteyn J., Smolinska A. Analysis of correlations between the occurrence of anti-MAP antibodies in blood serum and the presence of DNA-MAP in milk. Pol. J. Vet. Sci. 2009, 12:379-383.