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The Zoonotic Potential of Mycobacterium avium spp. paratuberculosis

A Systematic Review

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Abstract

Background

The zoonotic potential of Mycobacterium avium ssp. paratuberculosis (MAP) has been debated for almost a century because of similarities between Johne’s Disease (JD) in cattle and Crohn’s disease (CD) in humans. Our objective was to evaluate scientific literature investigating the potential association between these two diseases (MAP and CD) and the presence of MAP in retail milk or dairy products using a qualitative systematic review.

Method

The search strategy included 19 bibliographic databases, 8 conference proceedings, reference lists of 15 articles and contacting 28 topic-related scientists. Two independent reviewers performed relevance screening, quality assessment and data extraction stages of the review.

Results

Seventy-five articles were included. Among 60 case-control studies that investigated the association between MAP and CD, 37 were of acceptable quality. Twenty-three studies reported significant positive associations, 23 reported non-significant associations, and 14 did not detect MAP in any sample. Different laboratory tests, test protocols, types of samples and source populations were used in these studies resulting in large variability among studies. Seven studies investigated the association between CD and JD, two challenge trials reported contradictory results, one cross-sectional study did not support the association, and four descriptive studies suggested that isolated MAP is often closely related to cattle isolates. MAP detection in raw and pasteurized milk was reported in several studies.

Conclusions

Evidence for the zoonotic potential of MAP is not strong, but should not be ignored. Interdisciplinary collaboration among medical, veterinary and other public health officials may contribute to a better understanding of the potential routes of human exposure to MAP.

Résumé

Contexte

Le potentiel zoonotique de la paratuberculose aviaire (Mycobacterium avium ssp paratuberculosis–MAP) fait l’objet de débats depuis près d’un siècle en raison des similitudes entre la maladie de Johne (MJ) chez les bovins et la maladie de Crohn (MC) chez les humains. À l’aide d’un examen qualitatif systématique, nous avons évalué la documentation scientifique sur les liens éventuels entre ces deux maladies (le MAP et la MC) et la présence du MAP dans le lait ou les produits laitiers vendus au détail.

Méthode

Nous avons consulté 19 bases de données bibliographiques, les actes de 8 conférences et 15 articles cités en référence, et contacté 28 scientifiques spécialistes du sujet. Deux évaluateurs indépendants ont effectué un tri des documents selon leur pertinence, en ont évalué la qualité et ont extrait les données.

Résultats

Soixante-quinze articles ont été analysés. Sur les 60 études cas-témoins portant sur ‘association entre le MAP et la MC, 37 étaient de qualité acceptable. Vingt-trois études faisaient état d’associations significativement positives, 23 faisaient état d’associations non significatives, et 14 n’ont détecté le MAP dans aucun échantillon. Les études utilisaient différents essais de aboratoire, protocoles d’essai, types d’échantillons et populations sources, ce qui explique la très grande variabilité d’une étude à l’autre. Sept études portaient sur l’association entre la MC et la MJ, deux tests de provocation ont produit des résultats contradictoires, une étude transversale n’a pas confirmé d’association, et quatre études descriptives donnaient à penser que le MAP isolé est souvent étroitement lié aux isolats du bétail. Plusieurs études ont détecté le MAP dans du lait cru et pasteurisé.

Conclusion

Bien qu’elles ne soient pas concluantes, les preuves du potentiel zoonotique du MAP ne sont pas négligeables. Une collaboration interdisciplinaire entre les autorités de santé publique (médicales, vétérinaires et autres) pourrait contribuer à améliorer les connaissances des voies possibles d’exposition humaine au MAP.

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References

  1. Biet F, Boschiroli ML, Thorel MF, Guilloteau LA. Zoonotic aspects of Mycobacterium bovis and Mycobacterium avium-intracellulare complex (MAC). Vet Res 2005;36(3):411–36.

    Article  PubMed  Google Scholar 

  2. Inderlied CB, Kemper CA, Bermudez LE. The Mycobacterium avium complex. Clin Microbiol Rev 1993;6(3):266–310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Han XY, Tarrand JJ, Infante R, Jacobson KL, Truong M. Clinical significance and epidemiologic analyses of Mycobacterium avium and Mycobacterium intracellulare among patients without AIDS. J Clin Microbiol 2005;43(9):4407–12.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Ayele WY, Svastova P, Roubal P, Bartos M, Pavlik I. Mycobacterium avium subspecies paratuberculosis cultured from locally and commercially pasteurized cow’s milk in the Czech Republic. Appl Environ Microbiol 2005;71(3):1210–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Gao A, Mutharia L, Chen S, Rahn K. Odumeru J. Effect of pasteurization on survival of Mycobacterium paratuberculosis in milk. J Dairy Sci 2002;85(12):3198–205.

    Article  CAS  PubMed  Google Scholar 

  6. O’Doherty A, O’Grady D, Smith T, Egan J. Mycobacterium avium subsp. paratuberculosis in pasteurised and unpasteurised milk in the Republic of Ireland. Irish J Agr Food Res 2002;41(1):117–21.

    Google Scholar 

  7. Whittington RJ, Hope AF, Marshall DJ, Taragel CA, Marsh I. Molecular epidemiology of Mycobacterium avium subsp. paratuberculosis: IS900 restriction fragment length polymorphism and IS1311 polymorphism analyses of isolates from animals and a human in Australia. J Clin Microbiol 2000;38(9):3240–48.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Daniels MJ, Hutchings MR, Beard PM, Henderson D, Greig A, Stevenson K, et al. Do non-ruminant wildlife pose a risk of paratuberculosis to domestic livestock and vice versa in Scotland? J Wildl Dis 2003;39(1):10–15.

    Article  PubMed  Google Scholar 

  9. Grant IR. Zoonotic potential of Mycobacterium avium ssp. paratuberculosis: The current position. J Appl Microbiol 2005;98(6):1282–93.

    Article  CAS  PubMed  Google Scholar 

  10. Ghadiali AH, Strother M, Naser SA, Manning EJ, Sreevatsan S. Mycobacterium avium subsp. paratuberculosis strains isolated from Crohn’s disease patients and animal species exhibit similar polymorphic locus patterns. J Clin Microbiol 2004;42(11):5345–48.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kennedy DJ, Benedictus G. Control of Mycobacterium avium subsp. paratuberculosis infection in agricultural species. Rev Sci Tech 2001;20(1):151–79.

    Article  CAS  PubMed  Google Scholar 

  12. Chacon O, Bermudez LE, Barletta RG. Johne’s disease, inflammatory bowel disease, and Mycobacterium paratuberculosis. Annu Rev Microbiol 2004;58:329–63.

    Article  CAS  PubMed  Google Scholar 

  13. Harris JE, Lammerding AM. Crohn’s disease and Mycobacterium avium subsp. paratuberculosis: Current issues. J Food Prot 2001;64(12):2103–10.

    Article  CAS  PubMed  Google Scholar 

  14. Veterinary Services AU. Johnes Disease. Available online at: https://doi.org/www.aphis.usda.gov/vs/nahps/johnes/ (Accessed January 30, 2006).

  15. Hermon-Taylor J, El-Zaatari FAK. The Mycobacterium avium subspecies paratuberculosis problem and its relation to the causation of Crohn disease. In: Pedley S, Bartram J, World Health Organization, Pathogenesis Mycobacteria in Water: A Guide to Public Health Consequences, Monitoring and Management, 1st ed. London, UK: IWA Publishing on behalf of WHO, 2004;74–94.

    Google Scholar 

  16. Farrokhyar F, Swarbrick ET, Irvine EJ. A critical review of epidemiological studies in inflammatory bowel disease. Scand J Gastroenterol 2001;36(1):2–15.

    Article  CAS  PubMed  Google Scholar 

  17. Chiodini RJ, Van Kruiningen HJ, Thayer WR. Coutu JA. Spheroplastic phase of mycobacteria isolated from patients with Crohn’s disease. J Clin Microbiol 1986;24(3):357–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Thayer WR Jr., Coutu JA, Chiodini RJ, Van Kruiningen HJ, Merkal RS. Possible role of mycobacteria in inflammatory bowel disease. II. Mycobacterial antibodies in Crohn’s disease. Dig Dis Sci 1984;29(12):1080–85.

    Article  PubMed  Google Scholar 

  19. Ellingson JL, Anderson JL, Koziczkowski JJ, Radcliff RP, Sloan SJ, Allen SE, et al. Detection of viable Mycobacterium avium subsp. paratuberculosis in retail pasteurized whole milk by two culture methods and PCR. J Food Prot 2005;68(5):966–72.

    Article  CAS  PubMed  Google Scholar 

  20. Hruska K, Pavlik C. Paratuberculosis in Cattle: A Possible Risk for Consumers. International Conference, “Food Safety and Quality in Transition Countries”. Nitra, Slovakia, March 23–27, 2003.

    Google Scholar 

  21. Jones PH, Farver TB, Beaman B, Cetinkaya B. Morgan KL. Crohn’s Disease in people exposed to clinical cases of bovine paratuberculosis. Epidemiol Infect 2006;134(1):49–56.

    Article  CAS  PubMed  Google Scholar 

  22. Grant IR. Mycobacterium avium ssp. paratuberculosis in foods: Current evidence and potential consequences. Int J Dairy Technology 2006;59(2):112–17.

    Article  Google Scholar 

  23. Animal Health Australia. National Johne’s Disease Control Program (NJDCP). Available online at: https://doi.org/www.animalhealthaustralia.com.au/programs/jd/njdcp.cfm. (Accessed July 13, 2006).

    Google Scholar 

  24. Advisory Committee on the Microbiological Safety of Foods. Food Standards Agency Strategy for the Control of Mycobacterium avium subspecies Paratuberculosis (MAP) in Cows’ milk, 2003. Available online at: https://doi.org/www.food.gov.uk/multimedia/pdfs/acm_586.pdf (Accessed July 13, 2006).

    Google Scholar 

  25. Food Standards Agency. Strategy for the Control of Mycobacterium avium subspecies Paratuberculosis (MAP) in Cows Milk, 2003. Available online at: https://doi.org/www.food.gov.uk/multimedia/pdfs/map_strategy.pdf (Accessed July 13, 2006).

    Google Scholar 

  26. Pickup RW, Rhodes G, Arnott S, Sidi-Boumedine K, Bull TJ, Weightman A, et al. Mycobacterium avium subsp. paratuberculosis in the catchment area and water of the River Taff in South Wales, United Kingdom, and its potential relationship to clustering of Crohn’s disease cases in the city of Cardiff. Appl Environ Microbiol 2005;71(4):2130–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lehtola MJ, Torvinen E, Miettinen IT, Keevil CW. Fluorescence in situ hybridization using peptide nucleic acid probes for rapid detection of Mycobacterium avium subsp. avium and Mycobacterium avium subsp. paratuberculosis in potable-water biofilms. Appl Environ Microbiol 2006;72(1):848–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Rodriguez-Lazaro D, D’Agostino M, Herrewegh A, Pla M, Cook N, Ikonomopoulos J. Real-time PCR-based methods for detection of Mycobacterium avium subsp. paratuberculosis in water and milk. Int J Food Microbiol 2005;101(1):93–104.

    Article  CAS  PubMed  Google Scholar 

  29. Whan L, Ball HJ, Grant IR, Rowe MT. Occurrence of Mycobacterium avium subsp. paratuberculosis in untreated water in Northern Ireland. Appl Environ Microbiol 2005;71(11):7107–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Berghaus RD, Farver TB, Anderson RJ, Jaravata CC, Gardner IA. Environmental sampling for detection of Mycobacterium avium ssp. paratuberculosis on large California dairies. J Dairy Sci 2006;89(3):963–70.

    Article  CAS  PubMed  Google Scholar 

  31. Bernstein CN, Blanchard JF, Rawsthorne P, Collins MT. Population-based case control study of seroprevalence of Mycobacterium paratuberculosis in patients with Crohn’s disease and ulcerative colitis. J Clin Microbiol 2004;42(3):1129–35.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Arsenault J, Girard C, Dubreuil P, Daignault D, Galarneau JR, Boisclair J, et al. Prevalence of and carcass condemnation from maedi-visna, paratuberculosis and caseous lymphadenitis in culled sheep from Quebec, Canada. Prev Vet Med 2003;59(1–2):67–81.

    Article  PubMed  Google Scholar 

  33. Chamberlin W, Graham DY, Hulten K, El-Zimaity HM, Schwartz MR, Naser S, et al. Review article: Mycobacterium avium subsp. paratuberculosis as one cause of Crohn’s disease. Aliment Pharmacol Ther 2001;15(3):337–46.

    Article  CAS  PubMed  Google Scholar 

  34. Chiodini RJ. Crohn’s disease and the mycobac-terioses: A review and comparison of two disease entities. Clin Microbiol Rev 1989;2(1):90–117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Thompson DE. The role of mycobacteria in Crohn’s disease. J Med Microbiol 1994;41(2):74–94.

    Article  CAS  PubMed  Google Scholar 

  36. Morgan KL. Johne’s and Crohn’s. Chronic inflammatory bowel diseases of infectious aetiology? Lancet 1987;1(8540):1017–19.

    Article  CAS  PubMed  Google Scholar 

  37. Chiodini RJ, Rossiter CA. Paratuberculosis: A potential zoonosis? Vet Clin North Am Food Anim Pract 1996;12(2):457–67.

    Article  CAS  PubMed  Google Scholar 

  38. Jayarao BM, Shreekumar P. A meta-analytic study on the detection of Mycobacterium avium subsp. paratuberculosis from patients with Crohn’s Disease. [online] https://doi.org/www.Medjournal.com/ (Accessed July 1999).

    Google Scholar 

  39. Hruska K. Research on paratuberculosis: Analysis of publications 1994–2004. Vet Med (Praha) 2004;49(8):271–82.

    Article  Google Scholar 

  40. Gould G. Mycobacterium avium subsp. paratuberculosis (MAP) and the food chain. Emerging Pathogen Task Force, 2004.

    Google Scholar 

  41. Greenstein RJ. Is Crohn’s disease caused by a mycobacterium? Comparisons with leprosy, tuberculosis, and Johne’s disease. lancet Infect Dis 2003;3(8):507–14.

    Article  PubMed  Google Scholar 

  42. Collins MT. Paratuberculosis: Review of present knowledge. Acta Vet Scand 2003;44(3–4):217–21.

    PubMed  Google Scholar 

  43. Graham DY, Markesich DC, Yoshimura HH. Mycobacteria and inflammatory bowel disease. Results of culture. Gastroenterology 1987;92(2):436–42.

    Article  CAS  PubMed  Google Scholar 

  44. Millar D, Ford J, Sanderson J, Withey S, Tizard M, Doran T, et al. IS900 PCR to detect Mycobacterium paratuberculosis in retail supplies of whole pasteurized cows’ milk in England and Wales. Appl Environ Microbiol 1996;62(9):3446–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Moss MT, Sanderson JD, Tizard ML, Hermon-Taylor J, El-Zaatari FA, Markesich DC, et al. Polymerase chain reaction detection of Mycobacterium paratuberculosis and Mycobacterium avium subsp silvaticum in long term cultures from Crohn’s disease and control tissues. Gut 1992;33(9):1209–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Burnham WR, Lennard-Jones JE, Stanford JL. Bird RG. Mycobacteria as a possible cause of inflammatory bowel disease. Lancet 1978;2(8092 Pt 1):693–96.

    Article  CAS  PubMed  Google Scholar 

  47. Sargeant J, Amezcua R, Rajic A, Waddell L. Conducting Systematic Reviews in Agri-Food Public Health, 2005. Available online at: https://doi.org/www.fsrrn.net/UserFiles/File/conductingsysreviewsenglish[1].pdf (Accessed June 27, 2006).

    Google Scholar 

  48. Procite for windows 5.0 [Reference manager]. 5.0.3 version. ISI ResearchSoft Inc., 1995.

  49. SRS 3.0 [Electronic Systematic Review]. 3.0 version. Ottawa, ON: TrialStat Corporation, 2004.

  50. Dohoo I, Martin SW, Stryhn H. Veterinary Epidemiology Research, 1st ed. Prince Edward Island, Canada: Copyright The University of Prince Edward Island, 2003.

    Google Scholar 

  51. Van Kruiningen HJ, Chiodini RJ, Thayer WR, Coutu JA, Merkal RS, Runnels PL. Experimental disease in infant goats induced by a Mycobacterium isolated from a patient with Crohn’s disease. A preliminary report. Dig Dis Sci 1986;31(12):1351–60.

    Article  PubMed  Google Scholar 

  52. Gitnick G, Collins J, Beaman B, Brooks D, Arthur M, Imaeda T, et al. Preliminary report on isolation of mycobacteria from patients with Crohn’s disease. Dig Dis Sci 1989;34(6):925–32.

    Article  CAS  PubMed  Google Scholar 

  53. Motiwala AS, Strother M, Amonsin A, Byrum B, Naser SA, Stabel JR, et al. Molecular epidemiology of Mycobacterium avium subsp. paratuberculosis: Evidence for limited strain diversity, strain sharing, and identification of unique targets for diagnosis. J Clin Microbiol 2003;41(5):2015–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Francois B, Krishnamoorthy R, Elion J. Comparative study of Mycobacterium paratuberculosis strains isolated from Crohn’s disease and Johne’s disease using restriction fragment length polymorphism and arbitrarily primed polymerase chain reaction. Epidemiol Infect 1997;118(3):227–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Hutchinson B. Critical appraisal of review articles. Can Fam Phys 1993;39:1097–102.

    Google Scholar 

  56. Neely JG. Literature review articles as a research form. Otolaryngol Head Neck Surg 1993;108(6):743–48.

    Article  CAS  PubMed  Google Scholar 

  57. National Health and Medical Research Council. How to review the evidence: Systematic identification and review of the scientific literature. Australia: Commonwealth of Australia, 2000.

    Google Scholar 

  58. West S, King V, Carey TS, Lohr KN, McKoy N, Sutton SF, et al., prepared by the Research Triangle Institute–University of North Carolina Evidence-based Practice Center under Contract No. 290-97-0011. Systems to Rate the Strength of Scientific Evidence. Evidence Report/Technology Assessment No. 47: AHRQ Publication No. 02-E016. 2002.

    Google Scholar 

  59. Collins MT, Lisby G, Moser C, Chicks D, Christensen S, Reichelderfer M, et al. Results of multiple diagnostic tests for Mycobacterium avium subsp. paratuberculosis in patients with inflammatory bowel disease and in controls. J Clin Microbiol 2000;38(12):4373–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Al-Shamali M, Khan I, Al-Nakib B, Al-Hassan F, Mustafa AS. A multiplex polymerase chain reaction assay for the detection of Mycobacterium paratuberculosis DNA in Crohn’s disease tissue. Scand J Gastroenterol 1997;32(8):819–23.

    Article  CAS  PubMed  Google Scholar 

  61. Schwartz D, Shafran I, Romero C, Piromalli C, Biggerstaff J, Naser N, et al. Use of short-term culture for identification of Mycobacterium avium subsp. paratuberculosis in tissue from Crohn’s disease patients. Clin Microbiol Infect 2000;6(6):303–7.

    Article  CAS  PubMed  Google Scholar 

  62. Semret M, Turenne CY, Behr MA. Insertion sequence IS900 revisited. J Clin Microbiol 2006;44(3):1081–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Murray A, Oliaro J, Schlup MM, Chadwick VS. Mycobacterium paratuberculosis and inflammatory bowel disease: Frequency distribution in serial colonoscopic biopsies using the polymerase chain reaction. Microbios 1995;83(337):217–28.

    CAS  PubMed  Google Scholar 

  64. Sechi LA, Scanu AM, Molicotti P, Cannas S, Mura M, Dettori G, et al. Detection and isolation of Mycobacterium avium subspecies paratuberculosis from intestinal mucosal biopsies of patients with and without Crohn’s disease in Sardinia. Am J Gastroenterol 2005;100(7):1529–36.

    Article  PubMed  Google Scholar 

  65. Bull TJ, McMinn EJ, Sidi-Boumedine K, Skull A, Durkin D, Neild P, et al. Detection and verification of Mycobacterium avium subsp. paratuberculosis in fresh ileocolonic mucosal biopsy specimens from individuals with and without Crohn’s disease. J Clin Microbiol 2003;41(7):2915–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Ryan P, Bennett MW, Aarons S, Lee G, Collins JK, O’Sullivan GC, et al. PCR detection of Mycobacterium paratuberculosis in Crohn’s disease granulomas isolated by laser capture microdissection. Gut 2002;51(5):665–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Lisby G, Andersen J, Engbaek K, Binder V. Mycobacterium paratuberculosis in intestinal tissue from patients with Crohn’s disease demonstrated by a nested primer polymerase chain reaction. Scand J Gastroenterol 1994;29(10):923–29.

    Article  CAS  PubMed  Google Scholar 

  68. Fidler HM, Thurrell W, Johnson NM, Rook GA, McFadden JJ. Specific detection of Mycobacterium paratuberculosis DNA associated with granulomatous tissue in Crohn’s disease. Gut 1994;35(4):506–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Baksh FK, Finkelstein SD, Ariyanayagam-Baksh SM, Swalsky PA, Klein EC, Dunn JC. Absence of Mycobacterium avium subsp. paratuberculosis in the microdissected granulomas of Crohn’s disease. Mod Pathol 2004;17(10):1289–94.

    Article  PubMed  Google Scholar 

  70. Autschbach F, Eisold S, Hinz U, Zinser S, Linnebacher M, Giese T, et al. High prevalence of Mycobacterium avium subspecies paratuberculosis IS900 DNA in gut tissues from individuals with Crohn’s disease. Gut 2005;54(7):944–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Ikonomopoulos JA, Gorgoulis VG, Kastrinakis NG, Zacharatos PV, Kokotas SN, Evangelou K. et al. Sensitive differential detection of genetically related mycobacterial pathogens in archival material. Am J Clin Pathol 2000;114(6):940–50.

    Article  CAS  PubMed  Google Scholar 

  72. Noordhoek GT, Kolk AH, Bjune G, Catty D, Dale JW, Fine PE, et al. Sensitivity and specificity of PCR for detection of Mycobacterium tuberculosis: A blind comparison study among seven laboratories. J Clin Microbiol 1994;32(2):277–84.

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Navarro E, Fernandez JA, Escribano J, Solera J. PCR assay for diagnosis of human brucellosis. J Clin Microbiol 1999;37(5):1654–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. McFadden JJ, Fidler HM. Mycobacteria as possible causes of sarcoidosis and Crohn’s disease. Soc Appl Bacteriol Symp Ser 1996;25:47S–52S.

    Article  CAS  PubMed  Google Scholar 

  75. Sartor RB. Mechanisms of disease: Pathogenesis of Crohn’s disease and ulcerative colitis. Nature Clinical Practice Gastroenterology and Hepatology 2006;3(7):390–407.

    Article  CAS  PubMed  Google Scholar 

  76. Barratt HS, Kalantzis C, Polymeros D, Forbes A. Functional symptoms in inflammatory bowel disease and their potential influence in misclas-sification of clinical status. Aliment Pharmacol Ther 2005;21(2):l4l-47.

    Article  Google Scholar 

  77. Silverberg MS, Daly MJ, Moskovitz DN, Rioux JD, McLeod RS, Cohen Z, et al. Diagnostic misclassification reduces the ability to detect linkage in inflammatory bowel disease genetic studies. Gut 2001;49(6):773–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Sargeant J, Rajic A, Read S, Ohlsson A. The process of systematic review and its application in agri-food public-health. Prev Vet Med 2006;75(3–4):141–51.

    Article  CAS  PubMed  Google Scholar 

  79. Motiwala AS, Li LL, Kapur V, Sreevatsan S. Current understanding of the genetic diversity of Mycobacterium avium subsp paratuberculosis. Microbes Infection 2006;8(5):1406–18.

    Article  CAS  PubMed  Google Scholar 

  80. Rothman K, Greenland S. Modern Epidemiology, 2nd ed. Philadelphia, PA: Lippincott-Raven, 1998.

    Google Scholar 

  81. Suenaga K, Yokoyama Y, Okazaki K. Yamamoto Y. Mycobacteria in the intestine of Japanese patients with inflammatory bowel disease. Am J Gastroenterol 1995;90(1):76–80.

    CAS  PubMed  Google Scholar 

  82. Romero C, Hamdi A, Valentine JF, Naser SA. Evaluation of surgical tissue from patients with Crohn’s disease for the presence of Mycobacterium avium subspecies paratuberculosis DNA by in situ hybridization and nested polymerase chain reaction. Inflamm Bowel Dis 2005;11(2):116–25.

    Article  PubMed  Google Scholar 

  83. Sanderson JD, Moss MT, Tizard ML, Hermon-Taylor J. Mycobacterium paratuberculosis DNA in Crohn’s disease tissue. Gut 1992;33(7):890–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Dell’Isola B, Poyart C, Goulet O, Mougenot JF, Sadoun-Journo E, Brousse N, et al. Detection of Mycobacterium paratuberculosis by polymerase chain reaction in children with Crohn’s disease. J Infect Dis 1994;169(2):449–51.

    Article  PubMed  Google Scholar 

  85. Clarkston WK, Presti ME, Petersen PF, Zachary PE Jr, Fan WX, Leonardi CL, et al. Role of Mycobacterium paratuberculosis in Crohn’s disease: A prospective, controlled study using polymerase chain reaction. Dis Colon Rectum 1998;41(2):195–99.

    Article  CAS  PubMed  Google Scholar 

  86. Mishina D, Katsel P, Brown ST, Gilberts EC, Greenstein RJ. On the etiology of Crohn disease. Proc Natl Acad Sci USA 1996;93(18):98l6–20.

    Article  Google Scholar 

  87. Del Prete R, Quaranta M, Lippolis A, Giannuzzi V, Mosca A, Jirillo E, et al. Detection of Mycobacterium paratuberculosis in stool samples of patients with inflammatory bowel disease by Is900-based PCR and colori-metric detection of amplified DNA. J Microbiol Methods 1998;33(2):105–14.

    Article  Google Scholar 

  88. Yoshimura HH, Graham DY, Estes MK, Merkal RS. Investigation of association of mycobacteria with inflammatory bowel disease by nucleic acid hybridization. J Clin Microbiol 1987;25(1):45–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Hulten K, El-Zimaity HM, Karttunen TJ, Almashhrawi A, Schwartz MR, Graham DY, et al. Detection of Mycobacterium avium subspecies paratuberculosis in Crohn’s diseased tissues by in situ hybridization. Am J Gastroenterol 2001;96(5):1529–35.

    Article  CAS  PubMed  Google Scholar 

  90. Sechi LA, Mura M, Tanda E, Lissia A, Fadda G, Zanetti S. Mycobacterium avium sub. paratuberculosis in tissue samples of Crohn’s disease patients. New Microbiol 2004;27(1):75–77.

    CAS  PubMed  Google Scholar 

  91. McFadden J, Collins J, Beaman B, Arthur M, Gitnick G. Mycobacteria in Crohn’s disease: DNA probes identify the wood pigeon strain of Mycobacterium avium and Mycobacterium paratuberculosis from human tissue. J Clin Microbiol 1992;30(12):3070–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Bernstein CN, Nayar G, Hamel A, Blanchard JF. Study of animal-borne infections in the mucosas of patients with inflammatory bowel disease and population-based controls. J Clin Microbiol 2003;41(11):4986–90.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Rowbotham DS, Mapstone NP, Trejdosiewicz LK, Howdle PD, Quirke P. Mycobacterium paratuberculosis DNA not detected in Crohn’s disease tissue by fluorescent polymerase chain reaction. Gut 1995;37(5):660–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Naser SA, Ghobrial G, Romero C, Valentine JF. Culture of Mycobacterium avium subspecies paratuberculosis from the blood of patients with Crohn’s disease. lancet 2004;364(9439):1039–44.

    Article  PubMed  Google Scholar 

  95. Fujita H, Eishi Y, Ishige I, Saitoh K, Takizawa T, Arima T, et al. Quantitative analysis of bacterial DNA from Mycobacteria spp., Bacteroides vulgatus, and Escherichia coli in tissue samples from patients with inflammatory bowel diseases. J Gastroenterol 2002;37(7):509–16.

    Article  CAS  PubMed  Google Scholar 

  96. Chiba M, Kono M, Hoshina S, Komatsu M, Kitagawa Y, Iizuka M, et al. Presence of bacterial 16S ribosomal RNA gene segments in human intestinal lymph follicles. Scand J Gastroenterol 2000;35(8):824–31.

    Article  CAS  PubMed  Google Scholar 

  97. Kanazawa K, Haga Y, Funakoshi O, Nakajima H, Munakata A, Yoshida Y. Absence of Mycobacterium paratuberculosis DNA in intestinal tissues from Crohn’s disease by nested polymerase chain reaction. J Gastroenterol 1999;34(2):200–6.

    Article  CAS  PubMed  Google Scholar 

  98. Cellier C, De Beenhouwer H, Berger A, Penna C, Carbonnel F, Parc R, et al. Mycobacterium paratuberculosis and Mycobacterium avium subsp. silvaticum DNA cannot be detected by PCR in Crohn’s disease tissue. Gastroenterol Clin Biol 1998;22(8–9):675–78.

    CAS  PubMed  Google Scholar 

  99. Kallinowski F, Wassmer A, Hofmann MA, Harmsen D, Heesemann J, Karch H, et al. Prevalence of enteropathogenic bacteria in surgically treated chronic inflammatory bowel disease. Hepatogastroenterology 1998;45(23):1552–58.

    CAS  PubMed  Google Scholar 

  100. Riggio MP, Gibson J, Lennon A, Wray D, MacDonald DG. Search for Mycobacterium paratuberculosis DNA in orofacial granulomatosis and oral Crohn’s disease tissue by polymerase chain reaction. Gut 1997;41(5):646–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Frank TS, Cook SM. Analysis of paraffin sections of Crohn’s disease for Mycobacterium paratuberculosis using polymerase chain reaction. Mod Pathol 1996;9(1):32–35.

    CAS  PubMed  Google Scholar 

  102. Dumonceau JM, Van Gossum A, Adler M, Fonteyne PA, Van Vooren JP, Deviere J, et al. No Mycobacterium paratuberculosis found in Crohn’s disease using polymerase chain reaction. Dig Dis Sci 1996;41(2):421–26.

    Article  CAS  PubMed  Google Scholar 

  103. Kreuzpaintner G, Kirschner P, Wallner A, Kolble R, Hesterberg R, Thomas L, et al. Mycobacteria of Runyon groups I, II and IV do not play an aetiological role in Crohn’s disease. Eur J Gastroenterol Hepatol 1995;7(12):1177–82.

    Article  CAS  PubMed  Google Scholar 

  104. Ellingson JL, Cheville JC, Brees D, Miller JM, Cheville NF. Absence of Mycobacterium avium subspecies paratuberculosis components from Crohn’s disease intestinal biopsy tissues. Clin Med Res 2003;1(3):217–26.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Gibson J, Riggio M, McCreary C, Lennon A, Toner M. Looking for Mycobacterium paratuberculosis DNA by polymerase chain reaction (PCR) in orofacial granulomatosis (OFG) and oral Crohn’s disease tissue in an Irish population. Ir Med J 2000;93(7):218.

    CAS  PubMed  Google Scholar 

  106. Chiba M, Fukushima T, Horie Y, Iizuka M, Masamune O. No Mycobacterium paratuberculosis detected in intestinal tissue, including Peyer’s patches and lymph follicles, of Crohn’s disease. J Gastroenterol 1998;33(4):482–87.

    Article  CAS  PubMed  Google Scholar 

  107. Butcher PD, McFadden JJ, Hermon-Taylor J. Investigation of mycobacteria in Crohn’s disease tissue by Southern blotting and DNA hybridisation with cloned mycobacterial genomic DNA probes from a Crohn’s disease isolated mycobacteria. Gut 1988;29(9):1222–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Wall S, Kunze ZM, Saboor S, Soufleri I, Seechurn P, Chiodini R, et al. Identification of spheroplast-like agents isolated from tissues of patients with Crohn’s disease and control tissues by polymerase chain reaction. J Clin Microbiol 1993;31(5):1241–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Elsaghier A, Prantera C, Moreno C, Ivanyi J. Antibodies to Mycobacterium paratuberculosis-specific protein antigens in Crohn’s disease. Clin Exp Immunol 1992;90(3):503–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Naser SA, Hulten K, Shafran I, Graham DY, El-Zaatari FA. Specific seroreactivity of Crohn’s disease patients against p35 and p36 antigens of M. avium subsp. paratuberculosis. Vet Microbiol 2000;77(3–4):497–504.

    Article  CAS  PubMed  Google Scholar 

  111. Kobayashi K, Brown WR, Brennan PJ, Blaser MJ. Serum antibodies to mycobacterial antigens in active Crohn’s disease. Gastroenterology 1988;94(6):1404–11.

    Article  CAS  PubMed  Google Scholar 

  112. Olsen I, Wiker HG, Johnson E, Langeggen H, Reitan LJ. Elevated antibody responses in patients with Crohn’s disease against a 14-kDa secreted protein purified from Mycobacterium avium subsp. paratuberculosis. Scand J Immunol 2001;53(2):198–203.

    Article  CAS  PubMed  Google Scholar 

  113. El-Zaatari FA, Naser SA, Hulten K, Burch P, Graham DY. Characterization of Mycobacterium paratuberculosis p36 antigen and its seroreactivities in Crohn’s disease. Curr Microbiol 1999;59(2):115–19.

    Google Scholar 

  114. Suenaga K, Yokoyama Y, Nishimori I, Sano S, Morita M, Okazaki K, et al. Serum antibodies to Mycobacterium paratuberculosis in patients with Crohn’s disease. Dig Dis Sci 1999;44(6):1202–7.

    Article  CAS  PubMed  Google Scholar 

  115. Cohavy O, Harth G, Horwitz M, Eggena M, Landers C, Sutton C, et al. Identification of a novel mycobacterial histone H1 homologue (HupB) as an antigenic target of pANCA monoclonal antibody and serum immunoglobulin A from patients with Crohn’s disease. Infect Immun 1999;67(12):6510–17.

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Vannuffel P, Dieterich C, Naerhuyzen B, Gilot P, Coene M, Fiasse R, et al. Occurrence, in Crohn’s disease, of antibodies directed against a species-specific recombinant polypeptide of Mycobacterium paratuberculosis. Clin Diagn Lab Immunol 1994;1(2):241–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Walmsley RS, Ibbotson JP, Chahal H, Allan RN. Antibodies against Mycobacterium paratuberculosis in Crohn’s disease. QJM 1996;89(3):217–21.

    Article  CAS  PubMed  Google Scholar 

  118. Stainsby KJ, Lowes JR, Allan RN, Ibbotson JP. Antibodies to Mycobacterium paratuberculosis and nine species of environmental mycobacteria in Crohn’s disease and control subjects. Gut 1993;34(3):371–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Markesich DC, Sawai ET, Butel JS, Graham DY. Investigations on etiology of Crohn’s disease. Humoral immune response to stress (heat shock) proteins. Dig Dis Sci 1991;36(4):454–60.

    Article  CAS  PubMed  Google Scholar 

  120. McFadden JJ, Houdayer C. No evidence for antibodies to mycobacterial A60 antigen in Crohn’s disease sera by enzyme-linked immunoabsorbent assay (ELISA). J Med Microbiol 1988;25(4):295–98.

    Article  CAS  PubMed  Google Scholar 

  121. Matthews N, Mayberry JF, Rhodes J, Neale L, Munro J, Wensinck F, et al. Agglutinins to bacteria in Crohn’s disease. Gut 1980;21(5):376–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Ebert EC, Bhatt BD, Liu S, Das KM. Induction of suppressor cells by Mycobacterium paratuberculosis antigen in inflammatory bowel disease. Clin Exp Immunol 1991;83(2):320–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Rowbotham DS, Howdle PD, Trejdosiewicz LK. Peripheral cell-mediated immune response to mycobacterial antigens in inflammatory bowel disease. Clin Exp Immunol 1995;102(3):456–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Dalton HR, Hoang P, Jewell DP. Antigen induced suppression in peripheral blood and lamina propria mononuclear cells in inflammatory bowel disease. Gut 1992;33(3):324–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. O’Reilly CE, O’Connor L, Anderson W, Harvey P, Grant IR, Donaghy J, et al. 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(9):5138–44.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Grant IR, Ball HJ, Rowe MT. Incidence of Mycobacterium paratuberculosis in bulk raw and commercially pasteurized cows’ milk from approved dairy processing establishments in the United Kingdom. Appl Environ Microbiol 2002;68(5):2428–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Grant IR, Hitchings EI, McCartney A, Ferguson F, Rowe MT. 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(2):602–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Policy Advice and Effectiveness Program, Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, 160 Research Lane, Unit 206, Guelph, ON, N1G 5B2, Canada

    Lisa A. Waddell MSc, Andrijana Rajić DVM, MSc, PhD, Jan Sargeant DVM, PhD, Janet Harris BSc, Rocio Amezcua DVM, MSc, PhD, Lindsay Downey BSc & Susan Read DVM, MSc

  2. Department of Population Medicine, Ontario Veterinary College, University of Guelph, Canada

    Lisa A. Waddell MSc, Andrijana Rajić DVM, MSc, PhD & Scott A. McEwen DVM, DVSc

  3. Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton, ON, Canada

    Jan Sargeant DVM, PhD & Rocio Amezcua DVM, MSc, PhD

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  1. Lisa A. Waddell MSc
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  2. Andrijana Rajić DVM, MSc, PhD
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  8. Scott A. McEwen DVM, DVSc
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Correspondence to Lisa A. Waddell MSc.

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Acknowledgements: The authors thank Sandra Connors for her assistance with relevance screening, Dr. Marina Steele for assisting with the interpretation of immunology research and Dr. Mike Cassidy for his insightful comments and critical review.

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Waddell, L.A., Rajić, A., Sargeant, J. et al. The Zoonotic Potential of Mycobacterium avium spp. paratuberculosis. Can J Public Health 99, 145–155 (2008). https://doi.org/10.1007/BF03405464

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