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A review of bovine tuberculosis at the wildlife–livestock–human interface in sub-Saharan Africa

  • M. De GARINE-WICHATITSKY (a1) (a2), A. CARON (a1) (a2) (a3), R. KOCK (a4), R. TSCHOPP (a5) (a6) (a7), M. MUNYEME (a8), M. HOFMEYR (a9) and A. MICHEL (a10)...

Summary

Infection of wild animals by bovine tuberculosis (bTB) is raising concern worldwide. This article reviews the current epidemiological situation, risk of emergence and control options at the wildlife–livestock–human interface in sub-Saharan Africa. In livestock, bTB has been confirmed in the majority of countries from all parts of the continent. Wildlife infection is confirmed in seven countries from southern and eastern Africa, apparently spreading in the southern Africa region. Mycobacterium bovis has been isolated from 17 wild mammal species, although only four are suspected to play a role as maintenance host. Zoonotic risks are a concern, but no direct spillover from wildlife to humans has been documented, and no case of bTB spillback from wildlife to livestock has been confirmed. In this paper we assess the main risk factors of bTB spillover at the wildlife–livestock–human interface and suggest several research themes which could improve the control of the disease in the African context.

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Corresponding author

*Author for correspondence: Dr M. de Garine-Wichatitsky, CIRAD/RP-PCP, P.O. Box 1378, HarareZimbabwe. (Email: degarine@cirad.fr)

References

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1.Schmitt, SM, et al. Bovine tuberculosis in free-ranging white-tailed deer from Michigan. Journal of Wildlife Diseases 1997; 33: 749758.
2.Pfeiffer, DU. The role of a wildlife reservoir in the epidemiology of bovine tuberculosis: Massey University, 1994, 456 pp.
3.Delahay, RJ, The status of Mycobacterium bovis infection in UK wild mammals: a review. Veterinary Journal 2002; 164: 90105.
4.Aranaz, A, et al. Bovine tuberculosis (Mycobacterium bovis) in wildlife in Spain. Journal of Clinical Microbiology 2004; 42: 26022608.
5.Bengis, RG, et al. An outbreak of bovine tuberculosis in a free-living African buffalo (Syncerus caffer) population in the Kruger National Park: a preliminary report. Onderstepoort Journal of Veterinary Research 1996; 63: 1518.
6.De Lisle, GW, Mackintosh, CG, Bengis, RG. Mycobacterium bovis in free-living and captive wildlife, including farmed deer. Revue Scientifique et Technique de l'Office International des Epizooties 2001; 20: 86111.
7.Thoen, CO, et al. Tuberculosis: a re-emerging disease in animals and humans. Veterinaria Italiana 2009; 45: 135181.
8.Nolan, A, Wilesmith, JW. Tuberculosis in badgers (Meles meles). Veterinary Microbioogy 1994; 40: 179191.
9.Woodroffe, R, et al. Effects of culling on badger abundance: implications for tuberculosis control. Journal of Zoology 2008; 274: 28237.
10.Coleman, JD, Cooke, MM. Mycobacterium bovis infection in wildlife in New Zealand. Tuberculosis 2001; 81: 191202.
11.Ramsey, DSL, Efford, MG. Management of bovine tuberculosis in brushtail possums in New Zealand: predictions from a spatially explicit, individual-based model. Journal of Applied Ecology 2010; 47: 911919.
12.Paine, R, Martinaglia, G. Tuberculosis in wild buck living under natural conditions. Journal of Comparative Pathology and Therapeutics 1929; 42: 18.
13.Woodford, MH. Tuberculosis in wildlife in the Ruwenzori National Park, Uganda (Part II). Tropical Animal Health and Production 1982; 14: 155160.
14.De Vos, V, et al. The epidemiology of tuberculosis in free-ranging African buffalo (Syncerus caffer) in the Kruger National Park, South Africa. Onderstepoort Journal of Veterinary Research 2001; 68: 119130.
15.Smith, N, et al. European 1: a globally important clonal complex of Mycobacterium bovis. Infection, Genetics and Evolution 2011; 11: 13401351.
16.Müller, B, et al. African 1, an epidemiologically important clonal complex of Mycobacterium bovis dominant in Mali, Nigeria, Cameroon, and Chad. Journal of Bacteriology 2009; 191: 19511960.
17.Berg, S, et al. African 2: a clonal complex of Mycobacterium bovis epidemiologically important in East Africa. Journal of Bacteriology 2011; 193: 670678.
18.Brosch, R, et al. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proceedings of the National Academy of Sciences USA 2002; 99: 36843689.
19.Taylor, GM, et al. First report of Mycobacterium bovis DNA in human remains from the Iron Age. Microbiology 2007; 153: 12431249.
20.Hutcheon, D. Annual Report, Colonial Veterinary Surgeon. Cape of Good Hope, 1880.
21.Bengis, RG, Kock, RA, Fischer, J. Infectious animal disease: the wildlife livestock interface. Revue Scientifique et Technique de l'Office International des Epizooties 2002; 21: 5365.
22.Bradley, DG, et al. Genetics and domestic cattle origins. Evolutionary Anthropology 1998; 6: 7986.
23.Kock, RA. What is the infamous ‘wildlife/disease interface?’ A review of current knowledge for the African continent In: Osofsky, SA, Cleaveland, S, Karesh, WB et al. , eds. Conservation and Development Interventions at the Wildlife/Livestock Interface: Implications for Wildlife, Livestock and Human Health. Gland, Switzerland: IUCN, 2005, pp. 113.
24.Bengis, RG. Transfrontier conservation area initiatives in Sub-Saharan Africa: some animal health challenges. In: Osofsky, SA, Cleaveland, S, Karesh, WB et al. , eds. Conservation and Development Interventions at the Wildlife/Livestock Interface: Implications for Wildlife, Livestock and Human Health. Gland, Switzerland: IUCN, 2005, pp. 1519.
25.de Garine-Wichatitsky, M, et al. Consequences of animals crossing the edges of transfrontier parks. In: Andersson, JA, de Garine-Wichatitsky, M, Cumming, DHM, Dzingirai, V, Giller, KE, eds. Transfrontier Conservation Areas People Living on the Edge. New York and London: Earthscan, 2013, pp. 137162.
26.Nugent, G. Maintenance, spillover and spillback transmission of bovine tuberculosis in multi-host wildlife complexes: a New Zealand case study. Veterinary Microbiology 2011; 151: 3442.
27.Cosivi, O, et al. Epidemiology of Mycobacterium bovis infection in animals and humans, with particular reference to Africa. Revue Scientifique et Technique de l'Office International des Epizooties 1995; 14: 733746.
28.Michel, A, Müller, B, van Helden, P. Mycobacterium bovis at the animal-human interface: A problem, or not? Veterinary Microbiology 2009; 133: 335343
29.Michel, AL. Implications of tuberculosis in African wildlife and livestock. Annals of the New York Academy of Science 2002; 969: 251255.
30.Anon. World Animal Health Information Database (WAHID). World Organisation for Animal Health (OIE), 2012.
31.Anon. HANDISTATUS II. World Organisation for Animal Health (OIE), 2012.
32.Ayele, WY, et al. Bovine tuberculosis: an old disease but a new threat to Africa. International Journal of Tuberculosis and Lung Disease 2004; 8: 924937.
33.Boukary, AR, et al. Tuberculosis caused by Mycobacterium bovis in sub-Saharan Africa. Annales de Médecine Vétérinaire 2011; 155: 2337.
34.Gallagher, J, et al. Pulmonary tuberculosis in free-living lechwe antelope in Zambia. Tropical Animal Health and Production 1972; 4: 204213.
35.Michel, AL, et al. Wildlife tuberculosis in South African conservation areas: implications and challenges. Veterinary Microbiology 2006; 112: 91100.
36.Munyeme, M, et al. Tuberculosis in Kafue lechwe antelopes (Kobus leche kafuensis) of the Kafue Basin in Zambia. Preventive Veterinary Medicine 2010; 95: 305308.
37.de Garine-Wichatitsky, M, et al. Bovine tuberculosis in buffaloes, Southern Africa. Emerging Infectious Diseases 2010; 16: 884885.
38.Jori, F, et al. Assessment of the occurrence of bovine tuberculosis at the wildlife/livestock interface in two protected areas of Northern Botswana. International Wildlife TB Conference, Skukuza, Kruger National Park, 2012.
39.Alexander, KA, et al. Novel Mycobacterium tuberculosis complex pathogen, M. mungi. Emerging Infectious Diseases 2010; 16: 12961299.
40.Michel, AL, et al. Molecular epidemiology of Mycobacterium bovis isolates from free-ranging wildlife in South African game reserves. Veterinary Microbiology 2009; 133: 335343.
41.Michel, AL, Bengis, RG. The African buffalo: a villain for inter-species spread of infectious diseases in southern Africa. Onderstepoort Journal of Veterinary Research 2012; 79: 5.
42.Bengis, RG, et al. Bovine tuberculosis in free-ranging wildlife: a review of global occurrence, pathology and epidemiology of this disease, and potential conservation implications. International Wildlife TB Conference, Skukuza, Kruger National Park, 2012.
43.Woodford, MH. Tuberculosis in wildlife in the Ruwenzori National Park, Uganda (Part I). Tropical Animal Health and Production 1982; 14: 8188.
44.Michel, AL, et al. Bovine tuberculosis in African buffaloes: observations regarding Mycobacterium bovis shedding into water and exposure to environmental mycobacteria. BMC Veterinary Research 2007; 3: 23.
45.Tanner, M, Michel, AL. Investigation of the viability of M. bovis under different environmental conditions in the Kruger National Park. Onderstepoort Journal of Veterinary Research 1999; 66: 185190.
46.Ferguson, K, Hanks, J. A review of the environmental, social and economic impacts of game an veterinary fencing in Africa with particular reference to the Great Limpopo and Kavango-Zambezi Transfrontier Conservation Areas. Pretoria: Mammal Research Institute, 2010.
47.Caron, A, et al. Relationship between burden of infection in ungulate populations and wildlife/livestock interfaces. Epidemiology and Infection. Published online: 26 February 2013. doi:10.1017/S0950268813000204.
48.Norton-Griffiths, M. How many wildebeest do you need? World Economics 2007; 8: 4164.
49.Cleaveland, S, et al. Tuberculosis in Tanzanian wildlife. Journal of Wildlife Disease 2005; 41: 446453.
50.Tschopp, R, et al. Bovine tuberculosis in Ethiopian wildlife. Journal of Wildlife Disease 2010; 46: 7537562.
51.Cleaveland, S, et al. Mycobacterium bovis in rural Tanzania: risk factors for infection in human and cattle populations. Tuberculosis 2007; 87: 3043.
52.Wondewosen, T, et al. Conventional and molecular epidemiology of bovine tuberculosis in dairy farms in Addis Ababa city, the capital of Ethiopia. International Journal of Applied Research in Veterinary Medecine 2010; 8: 143151.
53.Oloya, J, et al. Risk factors for herd-level bovine-tuberculosis seropositivity in transhumant cattle in Uganda. Preventive Veterinary Medicine 2007; 80: 318329.
54.Oloya, J, et al. Mycobacteria causing human cervical lymphadenitis in pastoral communities in the Karamoja Region of Uganda. Epidemiology and Infection 2008; 136: 636643.
55.Asiimwe, BB, et al. Mycobacterium tuberculosis Uganda genotype is the predominant cause of TB in Kampala, Uganda. International Journal of Tuberculosis and Lung Disease 2008; 12: 386391.
56.Makita, K, et al. Evidence-based identification of the most important livestock related zoonotic diseases in Kampala, Uganda. Journal of Veterinary Medical Science 2011; 73: 9911000.
57.Firdessa, R, et al. Mycobacterial lineages causing pulmonary and extraulmonary tuberculosis in Ethiopia. Emerging Infectious Diseases (in press).
58.Gumi, B, et al. Zoonotic transmission of tuberculosis between pastoralists and their livestock in South-East Ethiopia. EcoHealth 2012; 9: 139149.
59.Tanner, M. Mycobacterium bovis in the wildlife-livestock-human interface of east and southern Africa. International Wildlife TB Conference, Skukuza, Kruger National Park, 2012.
60.Tarara, R, et al. Tuberculosis in wild olive baboons, Papio cynocephalus anubis (Lesson), in Kenya. Journal of Wildlife Diseases 1985; 21: 137140.
61.Goutard, F. Epidémiologie de la tuberculose et de la brucellose des bovins en zone périurbaine d'Abéché, Tchad. Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux 2002; 55: 513.
62.Schelling, E, et al. Molecular epidemiology of first mycobacteria isolates from animals in Chad. Epidémiologie et Santé Animale 2005; 48: 8191.
63.Ngandolo, BN, et al. Ante- and postmortem diagnostic of bovine tuberculosis from cattle at slaughterhouses in Southern Chad. Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux 2009; 62: 512.
64.Gidel, R, et al. A survey on bovine tuberculosis in several regions of Western Africa (Haute Volta and Côte d'Ivoire) using tuberculin tests. Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux 1969; 22: 337355.
65.Doutre, MP. Note on recent cases of bovine tuberculosis (Mycobacterium bovis) observed at Dakar's slaughterhouse. Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux 1976; 29: 309311.
66.Fofana, M. Bovine tuberculosis in Mali: results of an epidemiological survey of dairy farms from periurban areas in Bamako district. Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux 2003; 56: 115120.
67.Boukary, AR, et al. Bovine tuberculosis prevalence survey on cattle in the rural livestock system of Torodi (Niger). PLoS ONE 2011; 6: e24629.
68.Müller, B, et al. Molecular characterisation of Mycobacterium bovis isolated from cattle slaughtered at the Bamako abattoir in Mali. BMC Veterinary Research 2008; 4: 26.
69.Bonsu, OA, Laing, E, Akanmori, BD. Prevalence of tuberculosis in cattle in the Dangme-West district of Ghana, public health implications. Acta Tropica 2000; 76: 914.
70.Sidibé, SS, et al. Bovine tuberculosis in Mali: results of an epidemiological survey carried out in dairy farms from periurban areas in Bamako district. Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux 2003; 56: 115120.
71.Thorel, MF. Tuberculose. In: Principales Maladies Infectieuses et Parasitaires du Bétail, Europe et Régions Chaudes. Editions Médicales Internationales, Paris, France, 2003, pp. 927961.
72.Hibert, F, et al. Spatial avoidance of invading pastoral cattle by wild ungulates: insights from using point process statistics. Biodiversity and Conservation 2010; 19: 20032024.
73.Wittemyer, G, et al. Accelerated human population growth at protected area edges. Science 2008; 321 (123126).
74.Haydon, DT, et al. Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 2002; 8: 14681473.
75.Biet, F, Guilloteau, LA, Boschiroli, ML, Thorel, MF. Zoonotic aspects of Mycobacterium bovis and Mycobacterium avium-intracellulare complex (MAC). Veterinary Research 2005; 36: 411436.
76.Michel, AL, Müller, B, van Helden, P. Mycobacterium bovis at the animal-human interface: a problem, or not? Veterinary Microbiology 2010; 133: 335–43
77.Tschopp, R, et al. Repeated representative cross-sectional skin testing for bovine tuberculosis in cattle in traditional husbandry system in Ethiopia. Veterinary Record 2010; 167: 250256.
78.Humblet, M-F, Boschiroli, ML, Saegerman, C. Classification of worldwide bovine tuberculosis risk factors in cattle: a stratified approach. Veterinary Research 2009; 40: 50.
79.Kazwala, RR, et al. Isolation of Mycobacterium bovis from human cases of cervical adenitis in Tanzania: a cause for concern? International Journal of Tuberculosis and Lung Disease 2001; 5: 8791.
80.Tschopp, R, et al. Risk factors of bovine tuberculosis in cattle in rural livestock production systems of Ethiopia. Preventive Veterinary Medicine 2009; 89: 205211.
81.Gumi, B, et al. Prevalence of tuberculin reactors in pastoral cattle herds in the Oromia Region, Southern Ethiopia. Tropical Animal Health and Production 2011; 43: 10811087.
82.Mfinanga, SG, et al. Mycobacterial adenitis: role of Mycobacterium bovis, non-tuberculous mycobacteria, HIV infection, and risk factors in Arusha, Tanzania. East African Medical Journal 2004; 81: 171178.
83.Idigbe, EO, Anyiwo, CE, Onwujekwe, DI. Human pulmonary infections with bovine and atypical mycobacteria in Lagos, Nigeria. Journal of Tropical Medicine and Hygiene 1986; 89: 143148.
84.Mawak, JD, et al. Human pulmonary infections with bovine and environment (atypical) Mycobacteria in Jos, Nigeria. Ghana Medical Journal 2006; 40: 132136.
85.Rasolofo, Razanamparany V, et al. Prevalence of Mycobacterium bovis in human pulmonary and extra-pulmonary tuberculosis in Madagascar. International Journal of Tuberculosis and Lung Disease 1999; 3: 632634.
86.Mamo, G, et al. Pathology of camel tuberculosis and molecular characterization of its causative agents in pastoral regions of Ethiopia. PLoS ONE 2011; 6: e15862.
87.Paling, RW, et al. The occurrence of infectious diseases in mixed farming of domesticated wild herbivores and livestock in Kenya. II. Bacterial diseases. Journal of Wildlife Disease 1988; 24: 308316
88.Renwick, AR, White, PC, Bengis, RG. Bovine tuberculosis in southern African wildlife: a multi-species host-pathogen system. Epidemiology and Infection 2007; 135: 529540.
89.de Garine-Wichatitsky, M, et al. Measuring contacts between African buffalo and domestic cattle in the Great Limpopo Transfrontier Conservation Area: implications for modelling bovine tuberculosis spill-over between wild and domestic hosts. International Wildlife TB Conference, Skukuza, Kruger National Park, 2012.
90.Munyeme, M, et al. Prevalence of bovine tuberculosis and animal level risk factors for indigenous cattle under different grazing strategies in the livestock/wildlife interface areas of Zambia. Tropical Animal Health and Production 2009; 41: 345352.
91.Liss, GM, et al. Occupational exposure to Mycobacterium bovis infection in deer and elk in Ontario. Canadian Journal of Public Health 1994; 85: 326329.
92.Weyer, K, et al. Mycobacterium bovis as a zoonosis in the Kruger National Park, South Africa. International Journal of Tuberculosis and Lung Disease 1999; 3: 11131119.
93.Courtenay, O, et al. Is Mycobacterium bovis in the environment important for the persistence of bovine tuberculosis? Biology Letters 2006; 2: 460462.
94.Cooper, D. Bovine tuberculosis control in the Hluhluwe iMfolozi Park 1999–2012. International Wildlife TB Conference, Skukuza, Kruger National Park, 2012.
95.Cross, PC, et al. Disease, predation and demography: assessing the impacts of bovine tuberculosis on African buffalo by monitoring at individual and population levels. Journal of Applied Ecology 2009; 46: 467475.
96.Ferreira, S, Hofmeyr, M, Funston, P. The trouble with bovine tuberculosis and lions. International Wildlife TB Conference, Skukuza, Kruger National Park, 2012.
97.Omer, MK, et al. A cross-sectional study of bovine tuberculosis in dairy farms in Asmara, Eritrea. Tropical Animal Health and Production 2001; 33: 295303.
98.Ameni, G, Amenu, K, Tibbo, M. Bovine tuberculosis: prevalence and risk factor assessment in cattle and cattle owners in Wuchale-Jida district, Central Ethiopia. International Journal of Applied Research in Veterinary Medicine 2003; 1: 113.
99.Cook, AJC, et al. Human and bovine tuberculosis in the Monze district of Zambia – a cross-sectional study. British Veterinary Journal 1996; 152: 3746.
100.Firdessa, R, et al. High prevalence of bovine tuberculosis in dairy cattle in central Ethiopia: implications for the dairy industry and public health. PLoS ONE 2012; 7: e52851.
101.De Lisle, GW, et al. Tuberculosis in free-ranging wildlife: detection, diagnosis and management. Revue Scientifique et Technique de l'Office International des Epizooties 2002; 21: 317334.
102.Caron, A, Cross, PC, du Toit, JT. Ecological implications of bovine tuberculosis in African Buffalo herds. Ecological Applications 2003; 13: 13381345.
103.Caron, A, de Garine-Wichatitsky, M, Morand, S. Using the community of pathogens to infer inter-specific host epidemiological interactions at the wildlife/domestic interface. In: Morand, S, Beaudeau, F, Cabaret, J, eds. New Frontiers in Molecular Epidemiology of Infectious Diseases. Heidelberg: Springer, 2012, pp. 311332.
104.Hlokwe, TM, et al. Evaluation of the discriminatory power of variable number of tandem repeat (VNTR) typing of Mycobacterium bovis isolates from Kruger National Park. International Wildlife TB Conference, Skukuza, Kruger National Park, 2012.
105.Chambers, MA. Diagnostics. International Wildlife TB Conference, Skukuza, Kruger National Park, 2012.
106.Corner, LA, et al. Vaccination of European badgers (Meles meles) with BCG by the subcutaneous and mucosal routes induces protective immunity against endobronchial challenge with Mycobacterium bovis. Tuberculosis 2008; 88: 601609.
107.de Klerk, LM, Michel, A, Bengis, R, Kriek, N, Godfroid, J. BCG vaccination failed to protect yearling African buffaloes (Syncerus caffer) against experimental intratonsilar challenge with Mycobacterium bovis. Veterinary Immunology and Immunopathology 2010; 137: 8492.
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