Abstract
Wildlife tuberculosis (TB) is becoming one of the emerging challenges for conservation globally. South Asian region is home to many endangered species like Asian elephants, rhinoceros, and Bengal tigers. Although it carries more than one‐third of global burden of human TB, TB in livestock and wildlife has not been adequately studied. This chapter reviews the present knowledge and information about animal‐adapted members of Mycobacterium tuberculosis complex and wildlife TB in South Asia. Recent studies of TB from different wild animals in Nepal and Bangladesh have found that M.orygis is an emerging threat of wildlife TB in the region. These studies have demonstrated wide diversity of M. orygis strains circulating in the region indicating its endemic distribution. M. orygis–associated TB was discovered from a free‐ranging rhinoceros in Nepal and the finding could signify threat of TB in other wild animals, including a possibility of unknown maintenance host. Recent studies also revealed an emerging challenge caused by TB to elephants in different South Asian countries like Nepal, India, and Sri Lanka. Wildlife TB is becoming a conservation challenge in South Asia, but given the paucity of research in this area, it is overlooked and underexplored.
Keywords
- wildlife tuberculosis
- Mycobacterium tuberculosis complex
- Mycobacterium orygis
- Asian elephants
- South Asia
1. Introduction
South Asia or the South Asian Association for Regional Cooperation (SAARC) region consists of eight countries, namely, Afghanistan, Bangladesh, Bhutan, India, Maldives, Nepal, Pakistan, and Sri Lanka. This region is one of the world's hotspots for biodiversity as it includes 17 regions in the World Wildlife Fund (WWF)'s Global‐200 biodiverse ecoregions [1], and 2 of 25 priority regions for biodiversity conservation [2]. It is also considered as a high‐risk region for emerging infectious diseases that could originate in wildlife [3].
The
TB caused by
This study reviews the current knowledge and information about animal‐adapted members of the MTBC, the emerging threat of TB in wildlife, and the problem posed by TB to wildlife conservation in South Asia.
2. Animal‐adapted members of MTBC
With the advent of a suite of molecular methods for genotyping of the MTBC, such as spoligotyping, deletion typing, and genome sequencing, in combination with increasing veterinary awareness for wildlife conservation, we now have the opportunity to scientifically pursue TB in wildlife. As a result, many new members of MTBC have been identified and the findings have clearly contributed to our understanding of the MTBC and their wildlife reservoirs (Table 1). Increasingly wildlife are recognized as reservoirs of these MTBC organisms and these findings pose a threat to wildlife conservation, undermine livestock TB control programs, and provide another avenue for zoonotic transmission.
MTBC species | Reservoir host | Geographical area | References |
---|---|---|---|
European badger | UK and Ireland | [67] | |
Brush‐tailed possum | New Zealand | [31] | |
White‐tailed deer | North America | [29, 30] | |
Wild boar | Spain | [68] | |
African buffalo | South Africa | [34] | |
Lechwe | Zambia | [33] | |
Wild boar | Spain | [7] | |
Seal, sea lion | Australia, Argentina | [8] | |
Voles | UK | [9] | |
Antelopes*; deer, antelope§ | Middle east*;, South Asia§ | [10, 16§, 20§] | |
Meerkats | South Africa | [11, 39] | |
Dassie bacillus | Rock hyraxes | Southern Africa | [12, 36] |
Chimpanzee bacillus | Chimpanzee† | Ivory Coast | [14] |
The MTBC species
Historically, it was believed that human TB evolved from bovine TB as a zoonosis. The hypothesis for that belief was based on the characteristic of a wide host range for
3. M. orygis , an emerging MTBC and a conservation threat in South Asia
Before the use of molecular genotyping tools for differentiation of the members of the MTBC,
Host (number of isolates) | Geographical location | Wild/captive/domestic | References |
---|---|---|---|
Antelope (2) | Netherlands | Captive | [10] |
Water buck (3) | |||
Oryx (1) | |||
Antelope (1) | South Africa | ||
Deer (1) | United Kingdom | ||
Human (10) | South Asia | Not applicable | |
Human (1) | South East Asia | ||
African buffalo (1) | South Africa | Captive | [69] |
Cattle (1) | New Zealand | Domestic | [51] |
Human (1) | New Zealand/Indian Immigrant | Not applicable | |
Blue bull (1) | Nepal | Captive | [20] |
Spotted deer (1) | |||
Rhinoceros (1) | Wild | [16] | |
Monkey (2) | Bangladesh | Captive/wild captured | [21] |
Cattle (18) | Domestic |
We reported the isolation of
The greater one‐horned rhinoceros is the largest species of rhinoceros that is listed in Appendix I (most endangered) of the Convention on International Trade in Endangered Species (CITES), categorized as vulnerable by the International Union for Conservation of Nature (IUCN) Red List, and listed as a protected species by the Government of Nepal [44–46]. The present day free‐ranging population of rhinoceroses in Nepal and India has increased from only 600 individuals in 1975 to 3555 individuals by mid‐2015 [47]. In Nepal, the population of rhinoceroses is 645 individuals, of which 605 individuals live in CNP in a relatively narrow area of riverine grassland [48, 49]. From a conservation point of view, having a chronic and devastating disease like TB in this vulnerable and isolated population, that is already threatened from habitat destruction and poaching, is a matter of great concern for the animal's long‐term survival. Also, CNP is listed by the United Nations Educational, Scientific and Cultural Organization (UNESCO) as a World Heritage Site because of its rich biodiversity, being home to globally protected animals such as Bengal tigers
In a study in India, 16 postmortem tissue samples from 25 suspected TB cases of spotted deer from a zoo were positive for IS
4. M. orygis may be endemically distributed in South Asia
In a recent study we isolated 20
From our studies in Nepal and Bangladesh, we have identified five MLVA types, two types in Nepal and three types in Bangladesh, in different wild and domestic animals. In Nepal, we speculated that there may be an unknown reservoir host of
To the best of our knowledge, there are no confirmed diagnoses of
5. Elephant TB in South Asia
For centuries, elephants have been revered in Asia where they are the part of the region's culture and religion. They are seen as the guardians of forest, play a critical role to maintain the forest ecosystem, and are lately an indispensable asset for conservation work in Asia. Unfortunately, because of shrinking protected habitats and extensive poaching their numbers have declined and elephants are now classified as an endangered species [53]. As in other South Asian countries, elephants have sociocultural and economic value in Nepal [54]. However, elephants in Asia now face a potentially grave threat from TB.
TB in elephants is a reemerging disease caused primarily by
TB screening in Asian elephants (
There are about 200 captive elephants in Nepal that are used by government authorities for patrolling of protected areas, by the private sector for eco‐tourism, and in some cases for wildlife research projects [56]. TB was first reported in captive elephants in Nepal in CNP in 2002 [57] and from 2002 to 2014, more than 10 elephants died of TB in Nepal. A comprehensive study was conducted in Nepal for screening of TB in 115 captive elephants; the results show that 15 of 115 (13%) elephants were reactive on the Elephant TB Stat Pak® assay [58]. The Elephant TB Stat Pak® is a licensed serological test developed by ChemBio Diagnostics, Inc., Medford, NY, USA, that uses a cocktail of several selected
In 2007, a Nepal Elephant Healthcare and TB Surveillance Program was initiated to conduct regular screening of captive elephants. Similarly, in 2011, the Nepal Elephant Tuberculosis Control and Management Action Plan (2011–2015) was endorsed by the Government of Nepal providing detailed guidelines for the management of TB including the diagnosis and treatment of TB in elephants of Nepal [60]. This was the first elephant TB control action plan implemented in an Asian elephant range country.
A study conducted in India has shown that 15% of over 300 captive elephants tested were reactive on the Elephant TB Stat‐Pak® assay. The highest seroreactivity was among temple elephants; these elephants had the greatest contact with humans of the three management groups studied [23].
Although,
6. Other cases of TB in wildlife in South Asia
There are few reports of wildlife TB from South Asian countries. One study from a zoological collection in India reported TB in spotted deer [50], while a similar study in Pakistan reported TB in spotted deer and two antelopes, namely, chinkara gazella and black buck [62]. A few studies have reported TB from langur in India and rhesus monkey in Nepal [63, 64], and these may be associated with
7. Conclusion
In summary, in this review we have provided an overview of animal‐adapted members of the MTBC and indicated the role of wildlife as a reservoir host. In the future, the study of wildlife TB will not only be important for conservation efforts but also for finding potential novel subspecies of the MTBC. We also discussed in detail reports of
References
- 1.
Olson DM, Dinerstein E. The Global 200: Priority ecoregions for global conservation. Annals of the Missouri Botanical Garden. 2002;89(2):199–224. - 2.
Myers N, Mittermeler RA, Mittermeler CG, da Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403:853–858. - 3.
Morese SS, Mazet JAK, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana‐Torrelio C, Lipkin I, Daszak P. Prediction and prevention of the next pandemic zoonosis. The Lancet. 2012;380(9857):1956–1965. - 4.
Gordon SV, Behr MA. Comparative Mycobacteriology of the Mycobacterium tuberculosis complex. In: Mukundan H, Chambers M, Waters R, Larsen M, editors. Many Hosts of Mycobacteria: Tuberculosis, Leprosy, and other Mycobacterial Diseases of Man and Animals. Oxfordshire, UK: CAB International, 2015. - 5.
de Jong BC, Antonio M, Gagneux S. Mycobacterium africanum —review of an important cause of human tuberculosis in West Africa. PLoS Neglected Tropical Diseases. 2010;4:e744.http://dx.doi.org/10.1371/journal.pntd.0000744 - 6.
Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C, Eiglmeier K, Garnier T, Gutierrez C, Hewinson G, Kremer K, Parsons LM, Pym AS, Samper S, van Soolingen D, Cole ST. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proceeding of the National Academy of Science of the United States of America. 2002;19:3684–3689. - 7.
Rodriguez S, Bezos J, Romero B, de Juan L, Alvarez J, Castellanos E, Moya N, Lozano F, Javed MT, Saez‐Llorente JL, Liebana E, Mateos A, Dominguez L, Aranaz A. Mycobacterium caprae infection in livestock and wildlife, Spain. Emerging Infectious Disease. 2011;17:532–535. - 8.
Cousins DV, Bastida R, Cataldi A, Quse V, Redrobe S, Dow S, Duignan P, Murray A, Dupont C, Ahmed N, Collins DM, Butler WR, Dawson D, Rodriguez D, Loureiro J, Romano MI, Alito A, Zumarraga M, Bernardelli A. Tuberculosis in seals caused by a novel member of the Mycobacterium tuberculosis complex:Mycobacterium pinnipedii sp. nov. International Journal of Systematic and Evolutionary Microbiology. 2003;53:1305–1314. - 9.
Cavanagh R, Begon M, Bennett M, Ergon T, Graham IM, de Hass PEW, Hart CA, Koedam M, Kremer K, Lambin X, Roholl P, van Soolingen D. Mycobacterium microti infection (Vole tuberculosis in wild rodent populations. Journal of Clinical Microbiology. 2002;40:3281–3285. - 10.
van Ingen J, Rahim Z, Mulder A, Boeree MJ, Simeone R, Brosch R, van Soolingen D. Characterization of Mycobacterium orygis asM. tuberculosis complex subspecies. Emerging Infectious Disease. 2012;18:653–655. - 11.
Parsons SDC, Drewe JA, Nicolaas C, van Pittius G, Warren RM, van Helden PD. Novel cause of tuberculosis in Meerkats, South Africa. Emerging Infectious Disease. 2013;19:2004–2006. - 12.
Cousins DV, Peet RL, Gaynor WT, Williams SN, Gow BL. Tuberculosis in imported hyrax ( Procaviacapensis ) caused by an unusual variant belonging to theMycobacterium tuberculosis complex. Veterinary Microbiology. 1994;42:135–145. - 13.
Alexander KA, Laver PN, Michel AL, Williams M, van Helden PD, Warren RM, Gey van Pittius, NC. Novel Mycobacterium tuberculosis complex pathogen,M. mungi . Emerging Infectious Disease. 2010;16:1296–1299. - 14.
Coscolla M, Lewin A, Metzger S, Maetz‐Rennsing K, Calvignac‐Spencer S, Nitsche A, Dabrowski PW, Radonic A, Niemann S, Parkhill J, Couacy‐Hymann E, Feldman J, Comas I, Boesch C, Gagneux S, Leendertz FH. Novel Mycobacterium tuberculosis complex isolate from a wild chimpanzee. Emerging Infectious Disease. 2013;19:969–976. - 15.
de Lisle GW, Bengis RG, Schmitt SM,O’Brien DJ. Tuberculosis in free‐ranging wildlife: Detection, diagnosis and management. Revue Scientifiqueet Technique (International Office of Epizootics). 2002;21(2):317–334. - 16.
Thapa J, Paudel S, Sadaula A, Shah Y, Maharjan B, Kaufman GE, McCauley D, Gairhe KP, Tsubota T, Suzuki Y, Nakajima C. Mycobacterium orygis ‐associated tuberculosis in free‐ranging rhinoceros, Nepal, 2015. Emerging Infectious Disease. 2016;22(3):570–572. - 17.
STAC. SAARC epidemiological response on tuberculosis. SAARC Tuberculosis and HIV/AIDS Center, Kathmandu, Nepal, 2014. - 18.
Muller B, Salome D, Alonso S, Hattendorf J, Laisse CJM, Parsons SDC, van Helden PD, Zinsstag J. Zoonotic Mycobacterium bovis induced tuberculosis in humans. Emerging Infectious Disease. 2013;19:899–908. - 19.
Prasad HK, Singhal A, Mishra A, Shah NP, Katoch VM, Thakral SS, Singh DV, Chumber S, Bal S, Aggarwal S, Padma MV, Kumar S, Singh MK, Acharya SK. Bovine tuberculosis in India: Potential basis for zoonosis. Tuberculosis. 2005;85:421–428. - 20.
Thapa J, Nakajima C, Maharjan B, Poudel A, Suzuki Y. Molecular characterization of Mycobacterium orygis isolates from wild animals of Nepal. Japanese Journal of Veterinary Research. 2015;63(3):151–158. - 21.
Rahim Z, Thapa J, Fukushima Y, Suzuki H, van der Zanden, Adri GM, Gordon SV, Suzuki Y, Nakajima C. Tuberculosis caused by Mycobacterium orygis in dairy cattle and captured monkeys in Bangladesh: a new scenario of tuberculosis in South Asia. Transboundary and Emerging Diseases. 2016. DOI: 10.1111/tbed.12596. - 22.
Paudel S, Mikota SK, Nakajima C, Gairhe KP, Maharjan B, Thapa J, Poudel A, Shimozuru M, Suzuki Y, Tsubota T. Molecular characterization of Mycobacterium tuberculosis isolates from elephants of Nepal. Tuberculosis. 2014;94:287–292. doi: 10.1016/j.tube.2013.12.008 - 23.
Abraham D, Cheeran JV, Sukumar R, Mikota SK, Rao S, Ganguly S, Varma S. Health assessment of captive Asian elephants in India with special reference to tuberculosis. Report to Project Elephant, Ministry of Environment and Forests, Government of India, New Delhi, 2008. - 24.
Perera BVP, Salgadu MA, Gunawardena GSPS, Smith NH, Jinadasa HRN. First confirmed case of fatal tuberculosis in a Wild Sri Lankan elephant. Gajah. 2014;41:28–31. - 25.
Fitzgerald SD, Kaneene JB. Wildlife reservoirs of bovine tuberculosis worldwide: Hosts, pathology, surveillance and control. Veterinary Pathology. 2012;50:488–499. - 26.
Cosivi O, Grange JM, Daborn CJ. Zoonotic tuberculosis due to Mycobacterium bovis in developing countries. Emerging Infectious Disease. 1998;4:59–70. - 27.
Donnelly CA, Woodroffe R, Cox DR, Bourne J, Gettinby G, Le Fevre AM, McInerney JP, Morrison I. Impact of localized badger culling on tuberculosis incidence in British cattle. Nature. 2003;426:834–837. - 28.
Olea‐Popelka F, Flynn O, Costello E, McGrath GE, Collins JD, O’Keeffe JJ, Kelton DF, Berke O, Martin SW. Spatial relationship between Mycobacterium bovis strains in cattle and badgers in four areas in Ireland. Preventive Veterinary Medicine. 2005;71:57–70. - 29.
Carstensen M, DonCarlos MW. Preventing the establishment of a wildlife disease reservoir: A case study of bovine tuberculosis in Minnesota, USA. Veterinary Medicine International. 2011;2011:Article ID 413240, 10 p. - 30.
O’Brien DJ, Schmitt SM, Fitzgerald SD, Dale EB. Management of bovine tuberculosis in Michigan wildlife: Current status and near term prospects. Veterinary Microbiology. 2011;151:179–187. - 31.
Caley P, Hone J, Cowan PE. The relationship between prevalence of Mycobacterium bovis infection in feral ferrets and possum abundance. New Zealand Veterinary Journal. 2001;49:195–200. - 32.
Santos N, Correia-Neves M, Almeida V, Gortázar C. Wildlife Tuberculosis: A Systematic Review of the Epidemiology in Iberian Peninsula. In: Cunha M, editors, Epidemiology Insights. ISBN: 978-953-51-0565-7. Rijeka, Crotia: InTech, DOI: 10.5772/33781. 2012. Available from: http://www.intechopen.com/books/epidemiology-insights/wildlife-tuberculosis-a-systematic-review-of-theepidemiology-in-the-iberian-peninsula [Accessed: 2016-08-04]. - 33.
Hang’ombe MB, Munyeme M, Nakajima C, Fukushima Y, Suzuki H, Matandiko W, Ishii A, Mweene AS, Suzuki Y. Mycobacterium bovis infection at the interface between domestic and wild animals in Zambia. BMC Veterinary Research. 2012;8:221. - 34.
Michel AL, Bengis RG, Keet DF, Hofmeyr M, de Klerk LM, Cross PC, Jolles AE, Copper D, Whyte IJ, Buss P, Godfroid J. Wildlife tuberculosis in South African conservation areas: Implications and challenges. Veterinary Microbiology. 2006;112:91–100. - 35.
Miller M, Michel A, van Helden P, Buss P. Tuberculosis in rhinoceros: An under recognized threat? Transboundary and Emerging Diseases. 2016. DOI: 10.1111/tbed.12489 - 36.
Clarke C, van Helden P, Miller M, Parsons S. Animal‐adapted members of the Mycobacterium tuberculosis complex endemic to the southern Africa subregion. Journal of the South African Veterinary Association. 2016;87(1):a1322.http://dx.doi.org/10.4102/jsava.v87i1.1322 - 37.
Alexander KA, Pleydell E, Williams MC, Lane EP, Nyange JF, Michel, AL. Mycobacterium tuberculosis : An emerging disease of free‐ranging wildlife. Emerging Infectious Disease. 2002;8:598–601. - 38.
Alexander KA, Sanderson CE, Larsen MH, Robbe‐Austerman S, Williams MC, Palmer MV. Emerging tuberculosis pathogen hijacks social communication behavior in the group‐living banded mongoose ( Mungos mungo ). mBio. 2016;7(3):e00281–16. DOI:10.1128/mBio.00281‐16 - 39.
Dippenaar A, Parsons SDC, Sampson SL, van der Merwe RG, Drewe JA, Abdallah AM, Siame KK, Gey van Pittius NC, van Helden PD, Pain A, Warren RM. Whole genome sequence analysis of Mycobacterium suricattae . Tuberculosis. 2015;95:682–688. - 40.
van Soolingen D, de Hass PE, Haagsma J, Eger T, Hermans PWM, Ritacco V, Alito A, van Embden JDA. Use of various genetic markers in differentiation of Mycobacterium bovis strains from animals and humans and for studying epidemiology of bovine tuberculosis. Journal of Clinical Microbiology. 1994;32:2425–2433. - 41.
Mostowy S, Inwald J, Gordon S, Martin C, Warren R, Kremer K, Cousins D, Behr MA. Revisiting the evolution of Mycobacterium bovis . Journal of Bacteriology. 2005;187:6386–6395. - 42.
Huard RC, Fabre M, de Hass P, Lazzarini LCO, van Soolingen D, Cousins D, Ho JL. Novel genetic polymorphisms that further delineate the phylogeny of the Mycobacterium tuberculosis complex. Journal of Bacteriology. 2006;188:4271–4287. - 43.
Smith NH, Kremer K, Inwald J, Dale J, Driscoll JR, Gordon SV, van Soolingen D, Hewinson RG, Smith JM. Ecotypes of the Mycobacterium tuberculosis complex. Journal of Theoretical Biology. 2006;239:220–225. - 44.
Convention on International Trade in Endangered Species. Appendices [Internet]. 2015. Available from: https://www.cites.org/eng/app/appendices.php [Accessed: 2015‐11‐22]. - 45.
Talukdar BK, Emslie R, Bist SS, Choudhury A, Ellis S, Bonal BS, Malakar MC, Talukdar BN, Barula M. Rhinoceros unicornis . The IUCN Red List of Threatened Species 2008. 2008. e.T19496A8928657. Available from:http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T19496A8928657.en [Accessed: 2016‐08‐04]. - 46.
Department of National Park and Wildlife Conservation. Protected species (mammals) [Internet]. 2015. Available from: http://www.dnpwc.gov.np/protected_species/species/mammals [Accessed: 2015‐10‐30]. - 47.
World Wildlife Fund. Greater one horned rhino. 2015. Available from: http://http://wwf.panda.org/what_we_do/endangered_species/rhinoceros/asian_rhinos/indian_rhinoceros/ [Accessed: 2015‐10‐30]. - 48.
NTNC. National rhino count 2015: 645 individual rhinos in Nepal [Internet]. 2015. Available from: http://www.ntnc.org.np/news/national‐rhino‐count‐2015‐645‐individual‐rhinos‐nepal [Accessed: 2015‐10‐30]. - 49.
Subedi N, Jnawali SR, Dhakal M, Pradhan NMB, Lamichhane BR, Malla S, Amin R, Jhala YV. Population status, structure and distribution of the greater one‐horned rhinoceros Rhinocerosunicornis in Nepal. Oryx. 2013;47:352–360. - 50.
Sharma S, Mallick GP, Verma R, Ray SK. Polymerase chain reaction (PCR) amplification of IS6110 sequences to detect Mycobacterium tuberculosis complex from formalin‐fixed paraffin‐embedded tissue of deer (Axis axis ). Veterinary Research Communication. 2007;31:17–21. - 51.
Dawson KL, Bell A, Kawakami RP, Coley K, Yates G, Collins DM. Transmission of Mycobacteiumorygis (M. tuberculosis complex species) from a tuberculosis patient to a dairy cow in New Zealand. Journal of Clinical Microbiology. 2012;50:3136–3138. - 52.
Mahmud MAA, Belal SMSH, Shoshe NZ. Prevalence of bovine tuberculosis in cattle in the selected Upazila of Sirajganj district in Bangladesh. Bangladesh Journal of Veterinary Medicine. 2014;12:141–145. - 53.
World Wildlife Fund. Asian elephants. 2016. Available from: http://wwf.panda.org/what_we_do/endangered_species/elephants/asian_elephants/ [Accessed: 2016‐07‐18]. - 54.
Thapa J. Twin elephants born in Nepal. Gajah. 2009;30:53. - 55.
Mikota, SK, Lyashchenko KP, Lowenstine L, Agnew D, Maslow JN. Mycobacterial infections in elephants. In: Mukundan H, Chambers, MA, Waters WR, Larsen MH, editors, Many Hosts of Mycobacteria. Tuberculosis, Leprosy, and Other Mycobacterial Diseases of Man and Animals. CABI Publishing House, Nosworthy Way, Wallingford, UK, 2015. pp. 259–276. - 56.
Pradhan NMB, Williams AC, Dhakal M. Current status of Asian elephants in Nepal. Gajah. 2011;35:87–92. - 57.
Gairhe K. A case study of tuberculosis in captive elephants in Nepal. Report submitted to Department of National Parks and Wildlife Conservation, Kathmandu, Nepal, 2002. - 58.
Mikota SK, Gairhe K, Giri K, Hamilton K, Miller M, Paudel S, Lyashchenko K, Larsen RS, Payeur JB, Waters WR, Greenwald, Dumonceaux G, Vincent B, Kaufman GE. Tuberculosis surveillance of elephants ( Elephas maximus ) in Nepal at the captive‐wild interface. European Journal of Wildlife Research. 2015;61:221–229. - 59.
Lyashchenko KP, Greenwald R, Esfandiari J, Olsen JH, Ball R, Dumonceaux G, Dunker F, Buckley C, Richard M, Murray S, Payeur JB, Andersen P, Pollock JM, Mikota S, Miller M, Sofranko, Waters WR. Tuberculosis in elephants: Antibody responses to defined antigens of Mycobacterium tuberculosis , potential for early diagnosis, and monitoring of treatment. Clinical and Vaccine Immunology. 2006;13:722–732. - 60.
Nepal Elephant Tuberculosis Control and Management Action Plan (2011–2015). Government of Nepal, Ministry of Forests and Soil Conservation, Department of National Parks and Wildlife Conservation, Kathmandu, Nepal, 2011. - 61.
Zachariah A. Emerging diseases in the single largest Asian elephant ( Elephas maximus indicus ) population, Nilgiri Biosphere Reserve, South India. Report to United States Fish and Wildlife Service Asian Elephant Conservation Fund,2012. - 62.
Shahid AL, Javed MT, Khan MN, Cagiola M. Prevalence of bovine tuberculosis in zoo animals in Pakistan. Iranian Journal of Veterinary Research, Shiraz University. 2012;13:58–63. - 63.
Parmar SM, Jani RG, Kapadiya FM, Sutariya DR. Status of tuberculosis in the free living hanuman langur ( Presbytis entellus ) of Gujarat state. Indian Veterinary Journal. 2013;90:74–75. - 64.
Wilbur AK, Engel G, Rompis A, Putra IGAA, Lee BPYH, Aggimarangsee N, Chalise M, Shaw E, Oh G, Schillaci MA, Jones‐Engel L. From the mouths of monkeys: Detection of Mycobacterium tuberculosis complex DNA from buccal swabs of synanthropic Macaques. American Journal of Primatology. 2012;74:676–686. - 65.
Gordon SV, Bottai D, Simeone R, Stinear T, Brosch R. Pathogenicity in the tubercle bacillus: Molecular and evolutionary determinants. Bioessays. 2009;31:378–388. - 66.
Bos KI, Harkins KM, Herbig A, Coscolla M, Weber N, Comas I, Forrest SA, Bryant JM, Harris SR, Schuenemann VJ, Campbell TJ, Majander JK, Wilbur AK, Guichon RA, Steadman DLW, Cook DC, Niemann S, Behr MA, Zummarraga M, Bastida R, Huson D, Nieselt K, Young D, Parkhill J, Buikstra JE, Gagneux S, Stone AC, Krause J. Pre‐Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature. 2014;514:494–497. - 67.
Gallagher J, Clifton‐Hadley RS. Tuberculosis in badger: A review of the disease and its significance for other animals. Research in Veterinary Science. 2000;69:203–217. - 68.
Gracia‐Jimenez WL, Benuitez‐Medina JM, Fernandez‐Llario P, Abecia JA, Gracia‐Sanchez A, Martinez R, Risco D, Ortiz‐Pelaez A, Salguero FJ, Smith NH, Gomez L, Hermoso De Mendoza J. Comparative pathology of the natural infection by Mycobacterium bovis andMycobacterium caprae in wild boar (Susscrofa ). Transboundry and Emerging Disease. 2013;60:102–109. - 69.
Gey van Pittius NC, Perrett KD, Michel AL, Keet DF, Hlokwe T, Streicher EM, Warren RM, van Helden PD. Infection of African buffalo ( Synceruscaffer ) by oryx bacillus, a rare member of the antelope clade of theMycobacterium tuberculosis complex. Journal of Wildlife Disease. 2012;48:849–857.