Skip to main content Accessibility help
×
Home

The zoonotic potential of Mycobacterium avium ssp. paratuberculosis: a systematic review and meta-analyses of the evidence

  • L. A. WADDELL (a1) (a2), A. RAJIĆ (a3), K. D. C. STÄRK (a4) and S. A. McEWEN (a1)

Summary

This systematic review–meta-analysis appraises and summarizes all the available research (128 papers) on the zoonotic potential of Mycobacterium avium ssp. paratuberculosis. The latter has been debated for a century due to pathogenic and clinical similarities between Johne's disease in ruminants and Crohn's disease (108 studies) in humans and recently for involvement in other human diseases; human immunodeficiency virus (HIV) infection (2), sarcoidosis (3), diabetes mellitus type 1 (T1DM) (7) and type 2 (3), multiple sclerosis (5) and Hashimoto's thyroiditis (2). Meta-analytical results indicated a significant positive association, consistently across different laboratory methods for Crohn's disease [odds ratio (OR) range 4·26–8·44], T1DM (OR range 2·91–9·95) and multiple sclerosis (OR range 6·5–7·99). The latter two and the thyroiditis hypothesis require further investigation to confirm the association. Meta-regression of Crohn's disease studies using DNA detection methods indicated that choice of primers and sampling frame (e.g. general population vs. hospital-based sample) explained a significant proportion of heterogeneity. Other epidemiological studies demonstrated a lack of association between high-risk occupations and development of Crohn's disease. Due to knowledge gaps in understanding the role of M. paratuberculosis in the development or progression of human disease, the evidence at present is not strong enough to inform the potential public health impact of M. paratuberculosis exposure.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      The zoonotic potential of Mycobacterium avium ssp. paratuberculosis: a systematic review and meta-analyses of the evidence
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      The zoonotic potential of Mycobacterium avium ssp. paratuberculosis: a systematic review and meta-analyses of the evidence
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      The zoonotic potential of Mycobacterium avium ssp. paratuberculosis: a systematic review and meta-analyses of the evidence
      Available formats
      ×

Copyright

Corresponding author

* Author for correspondence: Ms. L. A. Waddell, Public Health Agency of Canada, 160 Research Lane, Unit 206, Guelph, Ontario N1G 5B2, Canada. (Email: lisa_waddell@phac-aspc.gc.ca)

References

Hide All
1. Behr, MA, Collins, DM (eds). Paratuberculosis: Organism, Disease, Control, 1st edn. UK: CAB International, 2010.
2. Biet, F, et al. Zoonotic aspects of Mycobacterium bovis and Mycobacterium avium-intracellulare complex (MAC). Veterinary Research 2005; 36: 411436.
3. Grant, IR. Zoonotic potential of Mycobacterium avium ssp. paratuberculosis: the current position. Journal of Applied Microbiology 2005; 98: 12821293.
4. Chiodini, RJ, et al. Spheroplastic phase of mycobacteria isolated from patients with Crohn's disease. Journal of Clinical Microbiology 1986; 24: 357363.
5. Chiodini, RJ. Crohn's disease and the mycobacterioses: a review and comparison of two disease entities. Clinical Microbiology Reviews 1989; 2: 90117.
6. Naser, SA, et al. Mycobacterium avium subspecies paratuberculosis causes Crohn's disease in some inflammatory bowel disease patients. World Journal of Gastroenterology 2014; 20: 74037415.
7. Nacy, C, Buckley, M. Mycobacterium avium paratuberculosis: Infrequent Human Pathogen or Public Health Threat? American Academy of Microbiology, Washington DC, USA, 2008.
8. Cossu, D, Masala, S, Sechi, LA. A Sardinian map for multiple sclerosis. Future Microbiology 2013; 8: 223232.
9. Sisto, M, et al. Proposing a relationship between Mycobacterium avium subspecies paratuberculosis infection and Hashimoto's thyroiditis. Scandinavian Journal of Infectious Diseases 2010; 42: 787790.
10. Paccagnini, D, et al. Linking chronic infection and autoimmune diseases: Mycobacterium avium subspecies paratuberculosis, SLC11A1 polymorphisms and type-1 diabetes mellitus. PLoS ONE 2009; 4: e7109.
11. Sechi, LA, et al. Mycobacterium avium subspecies paratuberculosis bacteremia in type 1 diabetes mellitus: an infectious trigger? Clinical Infectious Disease 2008; 46: 148149.
12. Molodecky, NA, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012; 142: 4654.
13. International Diabetes Federation. IDF Diabetes Atlas, 6th edn. International Diabetes Federation, 2013.
14. World Health Organisation. Atlas Multiple Sclerosis Resources in the World 2008. Geneva, Switzerland: World Health Organization, 2008.
15. Chronic thyroiditis (Hashimoto's disease) (http://www.ncbi.nlm.nih.gov/pubmedhealth/PMH0001409/). Accessed 25 July 2014.
16. Erdal, BS, et al. Unexpectedly high prevalence of sarcoidosis in a representative U.S. Metropolitan population. Respiratory Medicine 2012; 106: 893899.
17. El-Zaatari, FA, Osato, MS, Graham, DY. Etiology of Crohn's disease: the role of Mycobacterium avium paratuberculosis . Trends in Molecular Medicine 2001; 7: 247252.
18. Young, I, et al. The application of knowledge synthesis methods in agri-food public health: recent advancements, challenges and opportunities. Preventive Veterinary Medicine 2014; 113: 339355.
19. Sargeant, J, et al. The process of systematic review and its application in agri-food public-health. Preventative Veterinary Medicine 2006; 75: 141151.
20. Waddell, LA, et al. The zoonotic potential of Mycobacterium avium spp. paratuberculosis: a systematic review. Canadian Journal of Public Health 2008; 99: 145155.
21. Feller, M, et al. Mycobacterium avium subspecies paratuberculosis and Crohn's disease: a systematic review and meta-analysis. Lancet Infectious Diseases 2007; 7: 607613.
22. Abubakar, I, et al. Detection of Mycobacterium avium subspecies paratuberculosis from patients with Crohn's disease using nucleic acid-based techniques: a systematic review and meta-analysis. Inflammatory Bowel Disease 2008; 14: 401410.
23. Eltholth, MM, et al. Contamination of food products with Mycobacterium avium paratuberculosis: a systematic review. Journal of Applied Microbiology 2009; 107: 10611071.
24. Sargeant, J, et al. Conducting Systematic Reviews in Agri-Food Public Health, 2005 (http://www.angelfire.com/co4/civph/). Accessed 25 November 2014.
25. Rajic, A, Young, I, McEwen, SA. Improving the utilization of research knowledge in agri-food public health: a mixed-method review of knowledge translation and transfer. Foodborne Pathogens and Disease 2013; 10: 397412.
26. Harris, J, et al. Evaluating the effectiveness of search strategies for systematic reviews in zoonotic public health. In: Canadian Cochrane Symposium Proceedings. Edmonton: Canadian Cochrane. 2008, pp. 36.
27. Sohal, JS, et al. Strain diversity within Mycobacterium avium subspecies paratuberculosis – a review. Indian Journal of Experimental Biology 2010; 48: 716.
28. Rosenfeld, G, Bressler, B. Mycobacterium avium paratuberculosis and the etiology of Crohn's disease: a review of the controversy from the clinician's perspective. Canadian Journal of Gastroenterology 2010; 24: 619624.
29. Pierce, ES. Ulcerative colitis and Crohn's disease: is Mycobacterium avium subspecies paratuberculosis the common villain? Gut Pathogens 2010; 2: 21.
30. Lalande, J, Behr, MA. Mycobacteria in Crohn's disease: how innate immune deficiency may result in chronic inflammation. Expert Review of Clinical Immunology 2010; 6: 633641.
31. Kaevska, M, Hruska, K. Analysis of publications on paratuberculosis from 1995 to 2009 with emphasis on the period from 2005 to 2009. Veterinární Medicína 2010; 55: 4354.
32. Guyatt, G, et al. GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. Journal of Clinical Epidemiology 2011; 64: 383394.
33. Higgins, J, Altman, D. Assessing risk of bias in included studies, Chapter 8. In: Higgins, JPT, Green, S (eds). Cochrane Handbook for Systematic Reviews of Interventions Version 5.0·1 (updated September 2008). The Cochrane Collaboration, 2008.
34. Cochrane Handbook of Systematic Reviews and Interventions (http://handbook.cochrane.org/). Accessed 24 June 2014.
35. GRADE guidelines. best practices using the GRADE framework (http://www.gradeworkinggroup.org/publications/jce_series.htm). Accessed 24 June 2014.
36. Balshem, H, et al. GRADE guidelines: 3. Rating the quality of evidence. Journal of Clinical Epidemiology 2011; 64: 401406.
37. Guyatt, GH, et al. GRADE guidelines: 9. Rating up the quality of evidence. Journal of Clinical Epidemiology 2011; 64: 13111316.
38. Schunemann, H, et al. The GRADE approach and Bradford Hill's criteria for causation. Journal of Epidemiology and Community Health 2010; 65: 392395.
39. DerSimonian, R, Laird, N. Meta-analysis in clinical trials. Controlled Clinical Trials 1986; 7: 177188.
40. Higgins, JP, et al. Measuring inconsistency in meta-analyses. British Medical Journal 2003; 327: 557560.
41. Borenstein, M, et al. Introduction to Meta-Analysis . Chichester/Hoboken: John Wiley & Sons, 2009.
42. Egger, M, et al. Bias in meta-analysis detected by a simple, graphical test. British Medical Journal 1997; 315: 629634.
43. Begg, CB, Mazumdar, M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994; 50: 10881101.
44. Duval, S, Tweedie, R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000; 56: 455463.
45. Jones, PH, et al. Crohn's disease in people exposed to clinical cases of bovine paratuberculosis . Epidemiology and Infection 2006; 134: 4956.
46. Qual, DA, et al. Lack of association between the occurrence of Crohn's disease and occupational exposure to dairy and beef cattle herds infected with Mycobacterium avium subspecies paratuberculosis . Journal of Dairy Science 2010; 93: 23712376.
47. Wagner, J, et al. Mycobacterium avium subspecies paratuberculosis in children with early-onset Crohn's disease: a longitudinal follow-up study. Inflammatory Bowel Disease 2011; 17: 18251826.
48. Van Kruiningen, HJ, et al. Experimental disease in infant goats induced by a Mycobacterium isolated from a patient with Crohn's disease. A preliminary report. Digestive Diseases and Sciences 1986; 31: 13511360.
49. Gitnick, G, et al. Preliminary report on isolation of mycobacteria from patients with Crohn's disease. Digestive Diseases and Sciences 1989; 34: 925932.
50. Singh, AV, et al. Genotype profiles of Mycobacterium avium subspecies paratuberculosis recovered from suspected and Crohn's disease patients in India. Journal of Communicable Diseases 2010; 42: 91100.
51. Wynne, JW, et al. Exploring the zoonotic potential of Mycobacterium avium subspecies paratuberculosis through comparative genomics. PLoS ONE 2011; 6: e22171.
52. Ghadiali, AH, et al. Mycobacterium avium subsp. paratuberculosis strains isolated from Crohn's disease patients and animal species exhibit similar polymorphic locus patterns. Journal of Clinical Microbiology 2004; 42: 53455348.
53. Motiwala, AS, et al. Molecular epidemiology of Mycobacterium avium subsp. paratuberculosis: evidence for limited strain diversity, strain sharing, and identification of unique targets for diagnosis. Journal of Clinical Microbiology 2003; 41: 20152026.
54. Whittington, RJ, et al. 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. Journal of Clinical Microbiology 2000; 38: 32403248.
55. 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. Epidemiology and Infection 1997; 118: 227233.
56. Singh, SV, et al. Genotype profiles of Mycobacterium avium subspecies paratuberculosis isolates recovered from animals, commercial milk, and human beings in North India. International Journal of Infectious Diseases 2009; 13: e2217.
57. Sasikala, M, et al. Absence of Mycobacterium avium ssp. paratuberculosis-specific IS900 sequence in intestinal biopsy tissues of Indian patients with Crohn's disease. Indian Journal of Gastroenterology 2009; 28: 169174.
58. Magin, WS, Van Kruiningen, HJ, Colombel, JF. Immunohistochemical search for viral and bacterial antigens in Crohn's disease. Journal of Crohn's and Colitis 2013; 7: 161166.
59. Bibiloni, R, et al. The bacteriology of biopsies differs between newly diagnosed, untreated, Crohn's disease and ulcerative colitis patients. Journal of Medical Microbiology 2006; 55: 11411149.
60. Kanazawa, K, et al. Absence of Mycobacterium paratuberculosis DNA in intestinal tissues from Crohn's disease by nested polymerase chain reaction. Journal of Gastroenterology 1999; 34: 200206.
61. Gibson, J, et al. Looking for Mycobacterium paratuberculosis DNA by polymerase chain reaction (PCR) in orofacial granulomatosis (OFG) and oral Crohn's disease tissue in an Irish population. Irish Medical Journal 2000; 93: 218.
62. Fujita, H, et al. Quantitative analysis of bacterial DNA from Mycobacteria spp., Bacteroides vulgatus, and Escherichia coli in tissue samples from patients with inflammatory bowel diseases. Journal of Gastroenterology 2002; 37: 509516.
63. Kallinowski, F, et al. Prevalence of enteropathogenic bacteria in surgically treated chronic inflammatory bowel disease. Hepatogastroenterology 1998; 45: 15521558.
64. Chiba, M, et al. No Mycobacterium paratuberculosis detected in intestinal tissue, including Peyer's patches and lymph follicles, of Crohn's disease. Journal of Gastroenterology 1998; 33: 482487.
65. Al-Shamali, M, et al. A multiplex polymerase chain reaction assay for the detection of Mycobacterium paratuberculosis DNA in Crohn's disease tissue. Scandinavian Journal of Gastroenterology 1997; 32: 819823.
66. Dumonceau, JM, et al. No Mycobacterium paratuberculosis found in Crohn's disease using polymerase chain reaction. Digestive Diseases and Sciences 1996; 41: 421426.
67. Frank, TS, Cook, SM. Analysis of paraffin sections of Crohn's disease for Mycobacterium paratuberculosis using polymerase chain reaction. Modern Pathology 1996; 9: 3235.
68. Tanaka, K, et al. Mycobacterium paratuberculosis and Crohn's disease. Gut 1991; 32: 4345.
69. 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: 12221228.
70. Graham, DY, Markesich, DC, Yoshimura, HH. Mycobacteria and inflammatory bowel disease. Results of culture. Gastroenterology 1987; 92: 436442.
71. Sechi, LA, et al. Relationship between Crohn's disease, infection with Mycobacterium avium subspecies paratuberculosis and SLC11A1 gene polymorphisms in Sardinian patients. World Journal of Gastroenterology 2006; 12: 71617164.
72. Lozano-Leon, A, Barreiro-de, Acosta, Dominguez-Munoz, JE. Absence of Mycobacterium avium subspecies paratuberculosis in Crohn's disease patients. Inflammatory Bowel Diseases 2006; 12: 11901192.
73. Ellingson, JL, et al. Absence of Mycobacterium avium subspecies paratuberculosis components from Crohn's disease intestinal biopsy tissues. Clinical Medical Research 2003; 1: 217226.
74. Cellier, C, et al. Mycobacterium paratuberculosis and Mycobacterium avium subsp. silvaticum DNA cannot be detected by PCR in Crohn's disease tissue. Gastroenterologie Clinique et Biologique 1998; 22: 675678.
75. Shin, AR, et al. Identification of seroreactive proteins in the culture filtrate antigen of Mycobacterium avium ssp. paratuberculosis human isolates to sera from Crohn's disease patients. FEMS Immunology and Medical Microbiology 2010; 58: 128137.
76. Olsen, I, et al. Elevated antibody responses in patients with Crohn's disease against a 14-kDa secreted protein purified from Mycobacterium avium subsp. paratuberculosis . Scandinavian Journal of Immunology 2001; 53: 198203.
77. Vannuffel, P, et al. Occurrence, in Crohn's disease, of antibodies directed against a species-specific recombinant polypeptide of Mycobacterium paratuberculosis . Clinical and Diagnostic Laboratory Immunology 1994; 1: 241243.
78. Bach, H, et al. Immunogenicity of Mycobacterium avium subsp. paratuberculosis proteins in Crohn's disease patients. Scandinavian Journal of Gastroenterology 2011; 46: 3039.
79. Lee, A, et al. Association of Mycobacterium avium subspecies paratuberculosis With Crohn Disease in pediatric patients. Journal of Pediatric Gastroenterology and Nutrition 2011; 52: 170174.
80. Nakase, H, et al. Specific antibodies against recombinant protein of insertion element 900 of Mycobacterium avium subspecies paratuberculosis in Japanese patients with Crohn's disease. Inflammatory Bowel Diseases 2006; 12: 6269.
81. Kobayashi, K, et al. Serum antibodies to mycobacterial antigens in active Crohn's disease. Gastroenterology 1988; 94: 14041411.
82. Walmsley, RS, et al. Antibodies against Mycobacterium paratuberculosis in Crohn's disease. QJM 1996; 89: 217221.
83. Verdier, J, et al. Specific IgG response against Mycobacterium avium paratuberculosis in children and adults with Crohn's disease. PLoS ONE 2013; 8: e62780.
84. McFadden, JJ, Houdayer, C. No evidence for antibodies to mycobacterial A60 antigen in Crohn's disease sera by enzyme-linked immunoabsorbent assay (ELISA). Journal of Medical Microbiology 1988; 25: 295298.
85. Juste, RA, et al. Association between Mycobacterium avium subsp. paratuberculosis DNA in blood and cellular and humoral immune response in inflammatory bowel disease patients and controls. International Journal of Infectious Diseases 2009; 13: 247254.
86. Ebert, EC, et al. Induction of suppressor cells by Mycobacterium paratuberculosis antigen in inflammatory bowel disease. Clinical and Experimental Immunology 1991; 83: 320325.
87. Olsen, I, et al. Isolation of Mycobacterium avium subspecies paratuberculosis reactive CD4 T cells from intestinal biopsies of Crohn's disease patients. PLoS ONE 2009; 4: e5641.
88. Campos, N, et al. Macrophages from IBD patients exhibit defective tumour necrosis factor-alpha secretion but otherwise normal or augmented pro-inflammatory responses to infection. Immunobiology 2011; 216: 961970.
89. Sibartie, S, et al. Mycobacterium avium subsp. paratuberculosis (MAP) as a modifying factor in Crohn's disease. Inflammatory Bowel Diseases 2010; 16: 296304.
90. Clancy, R, et al. Molecular evidence for Mycobacterium avium subspecies paratuberculosis (MAP) in Crohn's disease correlates with enhanced TNF-alpha secretion. Digestive and Liver Diseases 2007; 39: 445451.
91. Singh, AV, et al. Evaluation of ‘indigenous absorbed ELISA kit’ for the estimation of seroprevalence of Mycobacterium avium subspecies paratuberculosis antibodies in human beings in North India. ISRN Veterinary Science 2011; 2011: 636038.
92. Rosu, V, et al. Specific immunoassays confirm association of Mycobacterium avium subsp. paratuberculosis with type-1 but not type-2 diabetes mellitus. PLoS One 2009; 4: e4386.
93. Bitti, ML, et al. Mycobacterium avium subsp. paratuberculosis in an Italian cohort of type 1 diabetes pediatric patients. Clinical and Developmental Immunology 2012; 2012: 785262.
94. Naser, SA, et al. Exploring the role of Mycobacterium avium subspecies paratuberculosis in the pathogenesis of type 1 diabetes mellitus: a pilot study. Gut Pathogens 2013; 5: 14.
95. Masala, S, et al. Sardinian type 1 diabetes patients, transthyretin and Mycobacterium avium subspecies paratuberculosis infection. Gut Pathogens 2012; 4: 24.
96. Cossu, A, et al. Antibodies recognizing specific Mycobacterium avium subsp. paratuberculosis's MAP3738c protein in type 1 diabetes mellitus children are associated with serum Th1 (CXCL10) chemokine. Cytokine 2013; 61: 337339.
97. Cossu, A, et al. MAP3738c and MptD are specific tags of Mycobacterium avium subsp. paratuberculosis infection in type I diabetes mellitus. Clinical Immunology 2011; 141: 4957.
98. Rani, PS, et al. Mycobacterium avium subsp. paratuberculosis is not discerned in diabetes mellitus patients in Hyderabad, India. International Journal of Medical Microbiology 2014; 304: 620625
99. Cossu, D, et al. Anti Mycobacterium avium subsp. paratuberculosis heat shock protein 70 antibodies in the sera of Sardinian patients with multiple sclerosis. Journal of the Neurological Sciences 2013; 335: 131133.
100. Frau, J, et al. Mycobacterium avium subsp. paratuberculosis and multiple sclerosis in Sardinian patients: epidemiology and clinical features. Multiple Sclerosis 2013; 19: 14371442.
101. Cossu, D, et al. Association of Mycobacterium avium subsp. paratuberculosis with multiple sclerosis in Sardinian patients. PLoS ONE 2011; 6: e18482.
102. Cossu, D, et al. Are Mycobacterium avium subsp. paratuberculosis and Epstein-Barr virus triggers of multiple sclerosis in Sardinia? Multiple Sclerosis 2012; 18: 11811184.
103. Cossu, D, et al. Association of Mycobacterium avium subsp. paratuberculosis and SLC11A1 polymorphisms in Sardinian multiple sclerosis patients. Journal of Infection in Developing Countries 2013; 7: 203207.
104. D'Amore, M, et al. Molecular identification of Mycobacterium avium subspecies paratuberculosis in an Italian patient with Hashimoto's thyroiditis and Melkersson-Rosenthal syndrome. Journal of Medical Microbiology 2010; 59: 137139.
105. Masala, S, et al. Recognition of zinc transporter 8 and MAP3865c homologous epitopes by hashimoto's thyroiditis subjects from Sardinia: a common target with type 1 diabetes? PLoS ONE 2014; 9: e97621.
106. Rosu, V, et al. Mycobacterium avium subspecies paratuberculosis is not associated with type-2 diabetes mellitus. Annals of Clinical Microbiology and Antimicrobials 2008; 7: 9.
107. Richter, E, et al. Mycobacterium avium subsp. paratuberculosis infection in a patient with HIV, Germany. Emerging Infectious Diseases 2002; 8: 729731.
108. Naser, SA, et al. Occurrence of the IS900 gene in Mycobacterium avium complex derived from HIV patients. Molecular and Cellular Probes 1999; 13: 367372.
109. El-Zaatari, FA, et al. Identification of Mycobacterium avium complex in sarcoidosis. Journal of Clinical Microbiology 1996; 34: 22402245.
110. Eishi, Y, et al. Quantitative analysis of mycobacterial and propionibacterial DNA in lymph nodes of Japanese and European patients with sarcoidosis. Journal of Clinical Microbiology 2002; 40: 198204.
111. Lisby, G, Milman, N, Jacobsen, GK. Search for Mycobacterium paratuberculosis DNA in tissue from patients with sarcoidosis by enzymatic gene amplification. Acta Pathologica Microbiologica et Immunologica Scandinavica 1993; 101: 876878.
112. Ebrahim, S, Clarke, M. STROBE: new standards for reporting observational epidemiology, a chance to improve. International Journal of Epidemiology 2007; 36: 946948.
113. von Elm, E, et al. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. British Medical Journal 2007; 335: 806808.
114. Vandenbroucke, JP, et al. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. Annals of Internal Medicine 2007; 147: W163194.
115. Del Prete, R, et al. Detection of Mycobacterium paratuberculosis in stool samples of patients with inflammatory bowel disease by IS900-based PCR and colorimetric detection of amplified DNA. Journal of Microbiological Methods 1998; 33: 105114.
116. Suenaga, K, et al. Serum antibodies to Mycobacterium paratuberculosis in patients with Crohn's disease. Digestive Diseases and Sciences 1999; 44: 12021207.
117. Kobayashi, K, Blaser, MJ, Brown, WR. Immunohistochemical examination for mycobacteria in intestinal tissues from patients with Crohn's disease. Gastroenterology 1989; 96: 10091015.
118. Bannantine, JP, Bermudez, LE. No holes barred: invasion of the intestinal mucosa by Mycobacterium avium subsp. paratuberculosis . Infection and Immunity 2013; 81: 39603965.
119. Bannantine, JP, et al. Complete genome sequence of Mycobacterium avium subsp. paratuberculosis, isolated from human breast milk. Genome Announcements 2014; 2: 10.1128/genomeA.01252-13.
120. Singh, SV, et al. Genome sequence of the ‘Indian Bison Type’ biotype of Mycobacterium avium subsp. paratuberculosis strain S5. Genome Announcements 2013; 1: 10.1128/genomeA.00005-13122.
121. Shankar, H, et al. 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. International Journal of Infectious Diseases 2010; 14: e1216.
122. Sohal, JS, et al. Genomic analysis of local isolate of Mycobacterium avium subspecies paratuberculosis . Veterinary Microbiology 2009; 134: 375382.
123. Dohoo, I, Martin, W, Stryn, H (eds). Methods in Epidemiologic Research. VER Inc., Charlottetown, Prince Edward Island, Canada, 2012.
124. Matthews, N, et al. Agglutinins to bacteria in Crohn's disease. Gut 1980; 21: 376380.
125. Markesich, DC, et al. Investigations on etiology of Crohn's disease. Humoral immune response to stress (heat shock) proteins. Digestive Diseases and Sciences 1991; 36: 454460.
126. Elsaghier, A, et al. Antibodies to Mycobacterium paratuberculosis-specific protein antigens in Crohn's disease. Clinical & Experimental Immunology 1992; 90: 503508.
127. Stainsby, KJ, et al. Antibodies to Mycobacterium paratuberculosis and nine species of environmental mycobacteria in Crohn's disease and control subjects. Gut 1993; 34: 371374.
128. Cohavy, O, 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. Infection and Immunity 1999; 67: 65106517.
129. Collins, MT, et al. Results of multiple diagnostic tests for Mycobacterium avium subsp. paratuberculosis in patients with inflammatory bowel disease and in controls. Journal of Clinical Microbiology 2000; 38: 43734381.
130. Bernstein, CN, et al. Population-based case control study of seroprevalence of Mycobacterium paratuberculosis in patients with Crohn's disease and ulcerative colitis. Journal of Clinical Microbiology 2004; 42: 11291135.
131. Bernstein, CN, et al. Testing the interaction between NOD-2 status and serological response to Mycobacterium paratuberculosis in cases of inflammatory bowel disease. Journal of Clinical Microbiology 2007; 45: 968971.
132. Polymeros, D, et al. Does cross-reactivity between Mycobacterium avium paratuberculosis and human intestinal antigens characterize Crohn's disease? Gastroenterology 2006; 131: 8596.
133. Singh, AV, et al. Presence and characterization of Mycobacterium avium subspecies paratuberculosis from clinical and suspected cases of Crohn's disease and in the healthy human population in India. International Journal of Infectious Diseases 2008; 12: 190197.
134. Di Sabatino, A, et al. Detection of Mycobacterium avium subsp. paratuberculosis (MAP)-specific IS900 DNA and antibodies against MAP peptides and lysate in the blood of Crohn's disease patients. Inflammatory Bowel Disease 2011; 17: 12541255.
135. Biet, F, et al. Serum antibodies to Mycobacterium avium subspecies paratuberculosis combined with anti-Saccharomyces cerevisiae antibodies in Crohn's disease patients: prevalence and diagnostic role. Digestive Diseases and Sciences 2011; 56: 17941800.
136. Rowbotham, DS, Howdle, PD, Trejdosiewicz, LK. Peripheral cell-mediated immune response to mycobacterial antigens in inflammatory bowel disease. Clinical and Experimental Immunology 1995; 102: 456461.
137. Dalton, HR, Hoang, P, Jewell, DP. Antigen induced suppression in peripheral blood and lamina propria mononuclear cells in inflammatory bowel disease. Gut 1992; 33: 324330.
138. Ren, Z, et al. Selective Th2 pattern of cytokine secretion in Mycobacterium avium subsp. paratuberculosis infected Crohn's disease. Journal of Gastroenterology and Hepatology 2008; 23: 310314.
139. Netea, MG, et al. Defective acute inflammation in Crohn's disease. Lancet 2006; 368: 577578.
140. Reid, JD, Chiodini, RJ. Serologic reactivity against Mycobacterium paratuberculosis antigens in patients with sarcoidosis. Sarcoidosis 1993; 10: 3235.

Keywords

Type Description Title
WORD
Supplementary materials

Waddell supplementary material
Appendix 1

 Word (309 KB)
309 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed