A review of infection of wildlife hosts with mycobacterium bovis and the diagnostic difficulties of the ‘no visible lesion’ presentation

New Zealand Veterinary Journal

Volumn 57, Issue 3, 2009, Pages 122-131

  Gavier Widen D ^a   Cooke, M M ^b   Gallagher, J ^c   Chambers, M A ^d   Gortazar C ^e  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b MASSEY UNIVERSITY   (New Zealand)

^c Truckle Park   (United Kingdom)

^d VETERINARY LABORATORIES AGENCY   (United Kingdom)

^e INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

Author keywords

Bovine tuberculosis; Brushtail possum (Trichosurus vulpecula); Cervids; Eurasian badger (Meles meles); European wild boar (Sus scrofa); Ferrets (Mustela furo); Mycobacterium bovis; Wildlife

Indexed keywords

ADENOID; ANIMAL; ANIMAL DISEASE; AUTOPSY; DIFFERENTIAL DIAGNOSIS; DISEASE CARRIER; DISEASE TRANSMISSION; ISOLATION AND PURIFICATION; LYMPH NODE; MICROBIOLOGY; MYCOBACTERIUM BOVIS; PALATINE TONSIL; PATHOLOGY; POLYMERASE CHAIN REACTION; REVIEW; TUBERCULOSIS; WILD ANIMAL;

ADENOIDS; ANIMALS; ANIMALS, WILD; AUTOPSY; DIAGNOSIS, DIFFERENTIAL; DISEASE VECTORS; LYMPH NODES; MYCOBACTERIUM BOVIS; PALATINE TONSIL; POLYMERASE CHAIN REACTION; TUBERCULOSIS;

BOVINAE; CERVIDAE; MELES MELES; MUSTELA; MUSTELA FURO; MYCOBACTERIUM BOVIS; PHALANGERIDAE; SUIDAE; SUS SCROFA; TRICHOSURUS; TRICHOSURUS VULPECULA;

EID: 68549105918     PISSN: 00480169     EISSN: 11760710     Source Type: Journal    
DOI: 10.1080/00480169.2009.36891     Document Type: Review

References (92)

1. Acevedo-Whitehouse K, Vicente J, Gortázar C, Höfle U, Fernández-de-Mera IG, Amos W. Genetic resistance to bovine tuberculosis in the Iberian wild boar. Molecular Ecology 14, 3209–17, 2005
2. Balseiro A, García Marín JF, Solano P, Garrido JM, Prieto JM. Histopathological classification of lesions observed in natural cases of paratuberculosis in free- ranging fallow deer (Dama dama). Journal of Comparative Pathology 138, 180–8, 2008
3. Bengis RG, Kriek NP, Keet DF, Raath JP, de Vos V, Huchzermeyer HF. An outbreak of bovine tuberculosis in a free-living African buffalo (Syncerus caffer Sparrman) population in the Kruger National Park: a preliminary report. Onderstepoort Journal ofVeterinary Research 63, 15–18, 1996
4. Bölske G, Englund L, Wahlström H, de Lisle GW Collins DM, Croston PS. Bovine tuberculosis in Swedish deer farms: Epidemiological investigations and tracing using restriction fragment analysis. Veterinary Record 136, 414–7, 1995
5. Bruning-Fann CS, Schmitt SM, Fitzgerald SD, Payeur JB, Whipple DL, Cooley TM, Carlson T, Friedrich P. Mycobacterium bovis in coyotes from Michigan. Journal of Wildlife Diseases 34, 632–6, 1998
6. Bruning-Fann CS, Schmitt SM, Fitzgerald SD, Fierke JS, Friedrich PD, Kaneene JB, et al. Bovine tuberculosis in free-ranging carnivores from Michigan. Journal ofWildlife Diseases 37, 58–64, 2001
7. Caley P, Hone J. Estimating the force of infection; Mycobacterium bovis infection in feral ferrets Mustela furo in New Zealand. Journal of Animal Ecology 71, 44–54, 2002
8. Caley P, Hone J. Assessing the host disease status of wildlife and the implications for disease control: Mycobacterium bovis infection in feral ferrets. Journal of Applied Ecology 42, 708–19, 2005
9. Cataloluk O, Cakmak EA, Buyukberber N, Barlas O. Formalin fixing and paraffin embedding may lead to extra band development in PCR. New Microbiologica 26, 193–8, 2003
10. Clancey JK. The incidence of tuberculosis in lechwe (Marsh Antelope). Tubercle 58, 151–6, 1997
11. Clifton-Hadley RS, Wilesmith JW. Tuberculosis in deer: A review. Veterinary Record 129, 5–12, 1991
12. Clifton-Hadley RS, Wilesmith JW Stuart FA. Mycobacterium bovis in the European badger (Meles meles): epidemiological findings in tuberculous badgers from a naturally infected population. Epidemiology and Infection 111, 9–19, 1993
13. Coleman JD. Distribution, prevalence, and epidemiology of bovine tuberculosis in brushtail possums, Trichosurus vulpecula, in the Hohonu Range, New Zealand. Australian Wildlife Research 15, 651–63, 1988
14. Coleman JD, Cooke MM. Mycobacterium bovis infection in wildlife in New Zealand. Tuberculosis 81, 191–202, 2001
15. Coleman JD, Jackson R, Cooke MM, Greuber L. Prevalence and spatial distribution of bovine tuberculosis in brushtail possums on a forest-scrub margin. New Zealand Veterinary Journal 42, 128–32, 1994
16. Cooke MM. Pathogenesis of tuberculosis in the brushtail possum, Trichosurus vulpecula. PhD thesis, Massey University, Palmerston North, NZ, 2000 a
17. Cooke MM. Tuberculosis sialoadenitis in a badger. New Zealand Veterinary Journal 48, 122, 2000 b
18. Cooke MM, Jackson R, Coleman JD, Alley MR. Naturally occurring tuberculosis caused by Mycobacterium bovis in brushtail possums (Trichosurus vulpecula): II. Pathology. New Zealand Veterinary Journal 43, 315–21, 1995
19. Corner LA. The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: how to assess the risk. Veterinary Microbiology 112, 303–12, 2006
20. Corner LA, Barrett RH, Lepper AWD, Lewis V Pearson CW A survey of mycobacteriosis of feral pigs in the Northern Territory. Australian Veterinary Journal 57, 537–42, 1981
21. Corner LA, Melville L, McCubbin K, Small KJ, McCormick BS, Wood PR, Rothel JS. Efficiency of inspection procedures for the detection of tuberculous lesions in cattle. Australian Veterinary Journal 67, 389–92, 1990
22. Crawshaw TR, Griffiths IB, Clifton-Hadley RS. Comparison of a standard and detailed postmortem protocol for detecting Mycobacterium bovis in badgers. Veterinary Record 163, 473–7, 2008
23. Davidson RM. The role of the opossum in spreading tuberculosis. New Zealand Journal of Agriculture 133, 21–5, 1976
24. Day T, O’Connor C, Matthews L. Possum social behaviour. In: Montague TL (ed). The Brushtail Possum. Biology, Impact and Management of an Introduced Marsupial Pp 35–46. Manaaki Whenua Press, Lincoln, NZ, 2000
25. Delahay RJ, De Leeuw ANS, Barlow AM, Clifton-Hadley RS, Cheeseman CL. The status of Mycobacterium bovis infection in UK wild mammals: a review. Veterinary Journal 164, 90–105, 2002
26. Delahay RJ, Smith GC, Barlow AM, Walker N, Harris A, Clifton-Hadley RS, Cheeseman CL. Bovine tuberculosis infection in wild mammals in the South-West region of England: A survey of prevalence and a semi-quantitative assessment of the relative risks to cattle. Veterinary Journal 173, 287–301, 2007
27. de la Rua-Domenech R, Goodchild AT, Vordermeier HM, Hewinson RG, Christiansen KH, Clifton-Hadley RS. Ante mortem diagnosis of tuberculosis in cattle: A review of the tuberculin tests, gamma interferon assay and other ancillary diagnostic techniques. Research in Veterinary Science 81, 190–210, 2006
28. de Lisle GW Mycobacterial infections in cats and dogs. Surveillance 20 (4), 24–6, 1993
29. de Lisle GW Mackintosh CG, Bengis RG. Mycobacterium bovis in free-living and captive wildlife, including farmed deer. Revue Scientifique de l’Office International des Epizooties 20, 86–111, 2001
30. de Lisle GW Yates GF, Caley P, Corboy RJ. Surveillance of wildlife for Mycobacterium bovis infection using culture of pooled tissue samples from ferrets (Mustela furo). New Zealand Veterinary Journal 53, 14–18, 2005
31. de Lisle GW, Kawakami RP, Yates GF, Collins DM. Isolation of Mycobacterium bovis and other mycobacterial species from ferrets and stoats. Veterinary Microbiology 132, 402–7, 2008
32. Ewer K, Millington KA, Deeks JJ, Alvarez L, Bryant G, Lalvani A. Dynamic antigen-specific T-cell responses after point-source exposure to Mycobacterium tuberculosis American Journal of Respiratory and Critical Care Medicine 174, 831–9, 2006
33. Fagan J. Tuberculosis in badgers in Ireland: Pathology. In: Hayden TJ (ed). The Badger. Pp 117–22. Royal Irish Academy, Dublin, Ireland, 1993
34. Fernandez-de-Mera IG, Perez de la Lastra JM, Ayoubi P, Naranjo V Kocan KM, Gortazar C, de la Fuente J. Differential expression of inflammatory and immune response genes in mesenteric lymph nodes of Iberian red deer (Cervus elaphus hispanicus) naturally infected with Mycobacterium bovis. Developmental and Comparative Immunology 32, 85–91, 2008
35. Francis J. Tuberculosis in Animals and Man: A Study in Comparative Pathology. Cassell & Co Ltd, London, UK, 1958
36. Gallagher J. The role of other animals in the epidemiology of tuberculosis in the badger. In: Lord Zuckerman (ed). Badgers, Cattle and Tuberculosis. Appendix VII. Pp 86–98. HMSO, London, UK, 1980
37. Gallagher J, Clifton-Hadley RS. Tuberculosis in badgers; a review of the disease and its significance for other animals. Research in Veterinary Science 69, 20317, 2000
38. Gallagher J, Muirhead RH, Burn KJ. Tuberculosis in wild badgers (Meles meles) in Gloucestershire: Pathology. Veterinary Record 98, 9–14, 1976
39. Gallagher J, Monies R, Gavier-Widen D, Rule B. Role of infected, nondiseased badgers in the pathogenesis of tuberculosis in the badger. Veterinary Record 142, 710–4, 1998
40. Gavier-Widen, D, Chambers MA, Palmer N, Newell DG, Hewinson RG. Pathology of natural Mycobacterium bovis infection in Eurasian badgers (Meles meles) and its relationship with bacterial excretion. Veterinary Record 148, 299–304, 2001
41. Gortazar C, Torres MJ, Vicente J, Acevedo P, Reglero M, de la Fuente J, Negro JJ, Aznar-Martin J. Bovine tuberculosis in Donana Biosphere Reserve: the role of wild ungulates as disease reservoirs in the last Iberian lynx strongholds. PLoS ONE3, e2776, doi:10.1371/journal.pone.0002776, 2008
42. Haddad N, Masselot M, Durand B. Molecular differentiation of Mycobacterium bovis isolates. Review of main techniques and applications. Research in Veterinary Science 76, 1–18, 2004
43. Heinmöller E, Renker B, Beyser K, Dietmaier W Langner C, Rüschoff J. Pitfalls in diagnostic molecular pathology- significance of sampling error. Virchows Archiv 439, 504–11, 2001
44. Hernandez-Pando R, Jeyanathan M, Mengistu G, Aguilar D, Orozco H, Harboe M, Rook GAW, Bjune G. Persistence of DNA from Mycobacterium tuberculosis in superficially normal lung tissue during latent infection. Lancet 356, 2133–7, 2000
45. Holt RD, Dobson AP, Begon M, Bowers RG, Schauber EM. Parasite establishment in host communities. Ecology Letters 6, 837–42, 2003
46. Hu Y, Henderson B, Lund PA, Tormay P, Ahmed MT, Gurcha SS, Besra GS, Coates ARM. A Mycobacterium tuberculosis mutant lacking the groEL homologue cpn60.1 is viable but fails to induce an inflammatory response in animal models of infection. Infection and Immunity 76, 1535–46, 2008
47. Jackson R, Cooke MM, Coleman JD, Morris RS. Naturally occurring tuberculosis caused by Mycobacterium bovis in brushtail possums (Trichosurus vulpecula): I. An epidemiological analysis of lesion distribution. New Zealand Veterinary Journal 43, 306–14, 1995
48. Jenkins HE, Morrison WI, Cox DR, Donnelly CA, Johnston WT, Bourne FJ, Clifton-Hadley RS, Gettinby G, McInerney JP, Watkins GH, Woodroffe R. The prevalence, distribution and severity of detectable pathological lesions in badgers naturally infected with Mycobacterium bovis. Epidemiology and Infection 30, 1–12, 2007
49. Kovalev GK. Tuberculosis in wildlife (Review). Journal of Hygiene, Epidemiology, Microbiology and Immunology 24, 495–502, 1980
50. Liebana E, Johnson L, Gough J, Durr P, Jahans K, Clifton-Hadley R, Spencer Y, Hewinson RG, Downs SH. Pathology of natural occurring bovine tuberculosis in England and Wales. Veterinary Journal 176, 354–60, 2008
51. Little TWA, Swan C, Thompson HV, Wilesmith JW. Bovine tuberculosis in domestic and wild mammals in an area of Dorset. 3. The prevalence of tuberculosis in mammals other than badgers and cattle. Journal of Hygiene (Cambridge) 89, 225–34, 1982
52. Lugton IW, Johnstone AC, Morris RS. Mycobacterium bovis infection in New Zealand hedgehogs (Erinaceus europaeus). New Zealand Veterinary Journal 43, 342–5, 1995
53. Lugton IW, Wobeser G, Morris RS, Caley P. Epidemiology of Mycobacterium bovis infection in feral ferrets (Mustela furo) in New Zealand: I. Pathology and diagnosis. New Zealand Veterinary Journal 45, 140–50, 1997
54. Lugton IW, Wilson PR, Morris RS, Nugent G. Epidemiology and pathogenesis of Mycobacterium bovis infection of red deer (Cervus elaphus) in New Zealand. New Zealand Veterinary Journal 46, 147–56, 1998
55. Mackintosh CG, Qureshi T, Waldrup K, Labes RE, Dodds KG, Griffin JF. Genetic resistance to experimental infection with Mycobacterium bovis in red deer (Cervus elaphus). Infection and Immunity 68, 1620–5, 2000
56. Martin-Atance P, Palomares F, Gonzalez-Candela M, Revilla E, Cubero MJ, Calzada J, Leon-Vizcaino L. Bovine tuberculosis in a free-ranging red fox (Vulpes vulpes) from Doñana National Park (Spain). Journal ofWildlife Diseases 41, 435–6, 2005
57. Martín-Hernando MP, Höfle U, Vicente J, Ruiz-Fons F, Vidal D, Barral M, Garrido JA, de la Fuente J, Gortazar C. Lesions associated with bovine tuberculosis infection in the European wild boar. Tuberculosis 87, 360–7, 2007
58. Martino PE, Martino JJ, Villar JA. Tuberculosis in mink. Veterinaria Argentina 24, 374–9, 1986
59. McInerney J, Small KJ, Caley P. Prevalence of Mycobacterium bovis infection in feral pigs in the Northern Territory. Australian Veterinary Journal 72, 448–51, 1995
60. Michel AL, Bengis RG, Keet DF, Hofmeys M, Klerk LM, Cross PC, Jolles AE, Cooper D, Whyte IJ, Buss P, Godfroid J. Wildlife tuberculosis in South African conservation areas: implications and challenges. Veterinary Microbiology 112, 91–100, 2006
61. Miller J, Jenny A, Rhyan J, Saari D, Suarez D. Detection of Mycobacterium bovis in formalin-fixed, paraffin-embedded tissues of cattle and elk by PCR amplification of an IS6110 sequence specific for Mycobacterium tuberculosis complex organisms. Journal of Veterinary Diagnostic Investigation 9, 244–9, 1997
62. Mitchison D. The virulence of tubercle bacilli from patients with pulmonary tuberculosis in India and other countries. Bulletin of the International Union Against Tuberculosis 35, 287–93, 1964
63. Muirhead RH, Gallagher J, Birn KJ. Tuberculosis wild badgers in Gloucestershire: Epidemiology. Veterinary Record 95, 552–5, 1974
64. Naranjo V, Ayoubi P, Vicente J, Ruiz-Fons F, Gortazar C, Kocan KM, de la Fuente J. Characterization of selected genes upregulated in non-tuberculous European wild boar as possible correlates of resistance to Mycobacterium bovis infection. Veterinary Microbiology 116, 224–31, 2006 a
65. Naranjo V Höfle U, Vicente J, Martín MP, Ruiz-Fons F, Gortazar C, Kocan KM, de la Fuente J. Genes differentially expressed in oropharyngeal tonsils and mandibular lymph nodes of tuberculous and nontuberculous European wild boars naturally exposed to Mycobacterium bovis. FEMS Immunology and Medical Microbiology 46, 298–312, 2006 b
66. Naranjo V, Gortazar C, Villar M, de la Fuente J. Comparative genomics and proteomics to study tissue-specific response and function in natural Mycobacterium bovis infections. Animal Health Research Reviews 8, 81–8, 2007
67. Naranjo V, Gortázar C, Vicente J, de la Fuente J. Evidence of the role of European wild boar as a reservoir of Mycobacterium tuberculosis complex. Veterinary Microbiology 127, 1–9, 2008
68. Nielsen SS, Toft N. Ante mortem diagnosis of paratuberculosis: A review of accuracy of ELISA, interferon-y assay and faecal culture techniques. Veterinary Microbiology 129, 217–35, 2008
69. Nishi JS, Shury T, Elkin BT. Wildlife reservoirs for bovine tuberculosis (Mycobacterium bovis) in Canada: Strategies for management and research. Veterinary Microbiology 112, 325–38, 2006
70. Nolan A. An investigation of the development of specific antibody responses of badgers (Meles meles) to infection with Mycobacterium bovis with reference to the pathogenesis and epidemiology of the disease. PhD thesis, Brunel University, West London, UK, 1991
71. Nolan A, Wilesmith JW. Tuberculosis in badgers (Meles meles). Veterinary Microbiology 40, 179–91, 1994
72. O’Brien DJ, Schmitt SM, Berry DE, Fitzgerald SD, Vanneste JR, Lyon TJ, Magsig D, Fierke JS, Cooley TM, Zwick LS, Thomsen BV. Estimating the true prevalence of Mycobacterium bovis in hunter-harvested white-tailed deer in Michigan. Journal ofWildlife Diseases 40, 42–52, 2004
73. O’Brien DJ, Schmitt SM, Fitzgerald SD, Berry DE, Hickling GJ. Managing the wildlife reservoir of Mycobacterium bovis: The Michigan, USA, experience. Veterinary Microbiology 112, 313–23, 2006
74. O’Neil BD, Pharo HJ. The control of bovine tuberculosis in New Zealand. New Zealand Veterinary Journal 43, 249–55, 1995
75. Pérez J, Calzada J, Leon-Vizcaino L, Cubero MJ, Velarde J, Mozos E. Tuberculosis in an Iberian lynx (Lynxpardina). Veterinary Record 148, 414–4, 2001
76. Pfeiffer DU, Hickling GJ, Morris RS, Patterson KP, Ryan TJ, Crews KB. The epidemiology of Mycobacterium bovis infection in brushtail possums (Trichosurus vulpecula Kerr) in the Hauhungaroa Ranges, New Zealand. New Zealand Veterinary Journal 43, 272–80, 1995
77. Qureshi T, Templeton JW Adams LG. Intracellular survival of Brucella abortus, Mycobacterium bovis BCG, Salmonella Dublin, and Salmonella typhimurium in macrophages from cattle genetically resistant to Brucella abortus. Veterinary Immunology andImmunopathology 50, 55–65, 1996
78. Ragg JR, Moller H, Waldrup KA. The prevalence of bovine tuberculosis (Mycobacterium bovis) infections in feral populations of cats (Felis catus), ferrets (Mustela Juro) and stoats (Mustela ermine) in Otago and Southland, New Zealand. New Zealand Veterinary Journal 43, 333–7, 1995 a
79. Ragg JR, Waldrup KA, Moller H. The distribution of gross lesions of tuberculosis caused by Mycobacterium bovis in feral ferrets (Mustela Juro) from Otago, New Zealand. New Zealand Veterinary Journal 43, 338–41, 1995 b
80. Renwick AR, White PC, Bengis RG. Bovine tuberculosis in southern African wildlife: a multi-species host-pathogen system. Epidemiology and Injection 135, 529–40, 2007
81. Reyes-García R, Perez-de-la-Lastra JM, Vicente J, Ruiz-Fons F, Garrido JM, Gortázar C. Large-scale ELISA testing of Spanish red deer for paratuberculosis. Veterinary Immunology and Immunopathology 124, 75–81, 2008
82. Rhyan JC, Saari DA. A comparative study of the histopathologic features of bovine tuberculosis in cattle, fallow deer (Dama dama), Sika deer (Cervus nippon), and red deer and elk (Cervus elaphus). Veterinary Pathology 32, 21520, 1995
83. Rich AR. Individual resistance. The influence of sex and age. The Pathogenesis oj Tuberculosis 2nd Edtn. Pp 182–251. CC Thomas, Springfield IL USA, 1951
84. Rohonczy EB, Balachandran AV, Dukes TW, Payeur JB, Rhyan JC, Saari DA, Whiting TL, Wilson SH, Jarnagin JL. A comparison of gross pathology, histopathology, and mycobacterial culture for the diagnosis of tuberculosis in elk (Cervus elaphus). Canadian Journal ofVeterinary Research 60, 108–14, 1996
85. Sangster C, Bergeson D, Lutze-Wallace C, Crichton V Wbbeser G. Feasibility of using coyotes (Canis latrans) as sentinels for bovine mycobacteriosis (Mycobacterium bovis) infection in wild cervids in and around Riding Mountain National Park, Manitoba, Canada. Journal oJ Wildlije Diseases 43, 432–8, 2007
86. Schmitt SM, Fitzgerald SD, Cooley TM, Brunning-Fann CS, Sullivan L, Berry D, Carlson NT, Minnis RB, Payeur JB, Sikarskie J. Bovine tuberculosis in free-ranging white-tailed deer from Michigan. Journal oJWildlije Diseases 33, 749–58, 1997
87. Shleeva MO, Bagramyan K, Telkov MV, Mukamolova GV Young M, Kell DB, Kaprelyants AS. Formation and resuscitation of ‘non-culturable’ cells of Rhodococcus rhodochrous and Mycobacterium tuberculosis in prolonged stationary phase. Microbiology 148, 1581–91, 2002
88. Sjogren I, Sutherland I. Studies of tuberculosis in man in relation to tuberculosis in cattle. Tubercle 56, 113–27, 1975
89. Une Y, Mori T. Tuberculosis as a zoonosis from a veterinary perspective. Comparative Immunology, Microbiology and Infectious Diseases 30, 415–25, 2007
90. Vicente J, Hofle U, Garrido JM, Fernández-de-Mera IG, Juste R, Barral M, Gortázar C. Wild boar and red deer display high prevalences of tuberculosislike lesions in Spain. Veterinary Research 37, 107–19, 2006
91. Vicente J, Hofle U, Fernández de Mera IG, Gortázar C. The importance of parasite life history and host density in predicting the impact of infections in red deer. Oecologia 152, 655–64, 2007
92. Vidal SM, Malo D, Vogan K, Skamene E, Gros P. Natural resistance to infection with intracellular parasites: isolation of a candidate for BCG. Cell 73, 469–85, 1993