Skip to main content Accessibility help
×
×
Home

Bronchoalveolar lavage for diagnosis of tuberculosis infection in elephants

  • R. Hermes (a1), J. Saragusty (a2), I. Moser (a3), S. Holtze (a1), J. Nieter (a3), K. Sachse (a3), T. Voracek (a4), A. Bernhard (a5), T. Bouts (a6), F. Göritz (a1) and T. B. Hildebrandt (a1)...

Abstract

Tuberculosis (TB) has been known to affect elephants for thousands of years. It was put into spotlight when few circus elephants were diagnosed carrying Mycobacterium (M.) tuberculosis. Because of the zoonotic risk and high susceptibility to M. tuberculosis, periodic testing was enacted since, in captive breeding programmes. Presently, trunk wash is the recommended diagnostic procedure for TB. Trunk wash, however, puts the operator at risk, has low sensitivity, and is prone to contamination. Here, bronchoalveolar lavage is described for the first time for TB diagnosis in elephants. Bronchial, trunk and mouth fluids were investigated using bacterial culture, M. tuberculosis complex (MTC)-specific real-time quantitative PCR (qPCR) and mycobacterial genus-specific qPCR for overall presence of mycobacteria or mycobacterial DNA including bacteria or DNA of closely related genera, respectively, in 14 elephants. Neither bacteria of the MTC nor their DNA were identified in any of the elephants. Yet, 25% of the cultures grew non-tuberculous mycobacteria (NTM) or closely related bacterial species. Furthermore, 85% of the samples contained DNA of NTM or closely related bacterial genera. This finding might explain continued false-positive results from various serological tests. From a zoonotic point of view, bronchoalveolar lavage is safer for the testing personal, has higher probability of capturing MTC and, through PCR, identifies DNA NTM in elephants. Yet, necessary endoscopic equipment, animal sedation and access to a TB reference laboratory might pose challenging requirements in remote conditions in some elephant range countries.

  • 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.

      Bronchoalveolar lavage for diagnosis of tuberculosis infection in elephants
      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.

      Bronchoalveolar lavage for diagnosis of tuberculosis infection in elephants
      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.

      Bronchoalveolar lavage for diagnosis of tuberculosis infection in elephants
      Available formats
      ×

Copyright

Corresponding author

Author for correspondence: Professor Dr Robert Hermes, E-mail: hermes@izw-berlin.de

References

Hide All
1. WHO (2016) Global Tuberculosis Report. Geneva, Switzerland: World Health Organization, pp. 1201.
2. Lécu, A and Ball, R (2011) Mycobacterial infections in zoo animals: relevance, diagnosis and management. International Zoo Yearbook 45, 183202.
3. Evans, GH (1910) Elephants and Their Diseases. Rangoon, Burma: The Government Press.
4. Iyer, AK (1937) Veterinary Science in India, ancient and modern with special reference to tuberculosis. Agricultre Livestock India 7, 718724.
5. Mikota, SK, Larsen, RS and Montali, RJ (2000) Tuberculosis in elephants in North America. Zoo Biology 19, 393403.
6. Montali, RJ, et al. (2001) Management aspects of herpesvirus infections and tuberculosis in elephants. In Schwammer, HM, Foose, TJ, Fouraker, M, Olson, D (eds). A Research Update on Elephants and Rhinos; Proceedings of the International Elephant and Rhino Research Symposium, Vienna. Münster, Germany: Schüling Verlag, pp. 8795.
7. Mikota, SK and Maslow, JN (2011) Tuberculosis at the human-animal interface: an emerging disease of elephants. Tuberculosis 91, 208211.
8. Abraham, D, Cheeran, JV and Mikota, SK (2010) Health assessment of captive Asian elephants (Elephas maximus) in India with special reference to Tuberculosis. In Kirk-Baer, C (ed.). Proceedings of the Association of American Zoo Veterinarians. South Padre Island, USA: Association of American Zoo Veterinarians, p. 229.
9. Verma-Kumar, S, et al. (2012) Serodiagnosis of tuberculosis in Asian elephants (Elephas maximus) in Southern India: a latent class analysis. PLoS ONE 7, e49548.
10. Fagen, A, Acharya, N and Kaufman, GE (2014) Positive reinforcement training for a trunk wash in Nepal's working elephants: demonstrating alternatives to traditional elephant training techniques. Journal of Applied Animal Welfare Science 17, 8397.
11. Mikota, SK, et al. (2007) Comparison of four serologic assays and culture to determine tuberculosis infection in captive elephants in Nepal. In: Kirk-Baer, C (ed.). Proceedings of the Association of American Zoo Veterinarians. Knoxville, USA: Association of American Zoo Veterinarians Knoxville, pp. 7172.
12. Ong, BL, et al. (2013) Tuberculosis in captive Asian elephants (Elephas maximus) in Peninsular Malaysia. Epidemiology and Infection 141, 14811487.
13. Yakubu, Y, et al. (2016) Evidence and potential risk factors of tuberculosis among captive Asian elephants and wildlife staff in Peninsular Malaysia. Preventive Veterinary Medicine 125, 147153.
14. Lassausaie, J, et al. (2014) Tuberculosis in Laos, who is at risk: the mahouts or their elephants? Epidemiology & Infection 143, 922931.
15. Obanda, V, et al. (2013) First reported case of fatal tuberculosis in a wild African elephant with past human-wildlife contact. Epidemiology and Infection 141, 14761480.
16. De Vos, V, et al. (2001) The epidemiology of tuberculosis in free-ranging African buffalo (Syncerus caffer) in the Kruger National Park, South Africa. Onderstepoort Journal of Veterinary Research 68, 119130.
17. Miller, M, et al. (2015) Antemortem diagnosis of Mycobacterium bovis infection in free-ranging African lions (Panthera leo) and implications for transmission. Journal of Wildlife Diseases 51, 493497.
18. Renwick, AR, White, PCL and Bengis, RG (2007) Bovine tuberculosis in southern African wildlife: a multi-species host–pathogen system. Epidemiology and Infection 135, 529540.
19. Lyashchenko, KP, et al. (2006) Tuberculosis in elephants: antibody responses to defined antigens of Mycobacterium tuberculosis, potential for early diagnosis, and monitoring of treatment. Clinical Vaccine Immunology 13, 722732.
20. Yong, H, et al. (2011) Disseminated infection due to Mycobacterium avium Subsp. avium in an Asian elephant (Elephas maximus). Journal of Zoo and Wildlife Medicine 42, 743746.
21. Lacasse, C, et al. (2007) Two cases of atypical mycobacteriosis caused by Mycobacterium szulgai associated with mortality in captive African elephants (Loxodonta africana). Journal of Zoo and Wildlife Medicine 38, 101107.
22. Shojaei, H, et al. (2000) Mycobacterium elephantis sp. nov., a rapidly growing non-chromogenic Mycobacterium isolated from an elephant. International Journal of Systematic and Evolutionary Microbiology 50, 18171820.
23. Holt, N (2015) The infected elephant in the room. Slate. Available at http://www.slate.com/blogs/wild_things/2015/03/24/elephant_tuberculosis_epidemic_zoo_and_circus_animals_passing_tb_to_humans.html (Accessed 03 August 2015). (Archived by WebCite® at http://www.webcitation.org/6aV8W1wJR).
24. Kik, M, et al. Mycobacterium tuberculosis infection in two African elephants (Loxodonta africana). In Szentiks, CA, Schumann, A (eds). Proceedings of the International Conference on Diseases of Zoo and Wild Animals. Barcelona: Leibniz Institute for Zoo and Wildlife Research, 2015, p. 10.
25. Michalak, K, et al. (1998) Mycobacterium tuberculosis infection as a zoonotic disease: transmission between humans and elephants. Emerging Infectious Diseases 4, 283287.
26. Murphree, R, et al. (2011) Elephant-to-human transmission of tuberculosis, 2009. Emerging Infectious Diseases 17, 366371.
27. Stephens, N, et al. (2013) Transmission of Mycobacterium tuberculosis from an Asian elephant (Elephas maximus) to a chimpanzee (Pan troglodytes) and humans in an Australian zoo. Epidemiology and Infection 141, 14881497.
28. Une, Y and Mori, T (2007) Tuberculosis as a zoonosis from a veterinary perspective. Comparative Immunology and Microbiology 30, 415425.
29. Zlot, A, et al. (2016) Diagnosis of Tuberculosis in Three Zoo Elephants and A Human Contact – Oregon 2013. Washington, DC, USA: US Department of Health and Human Services/Centers for Disease Control and Prevention, pp. 3981402.
30. Angkawanish, T, et al. (2010) Mycobacterium tuberculosis infection of domesticated Asian elephants, Thailand. Emerging Infectious Diseases 16, 19491951.
31. Perera, BVP, et al. (2015) First confirmed case of fatal tuberculosis in a wild Sri Lankan elephant (Elephas maximus maximus) caused by Mycobacterium tuberculosis . In Szentiks, CA, Schumann, A (eds.). Proceedings of the International Conference on Diseases of Zoo and Wild Animals. Barcelona: Leibniz Institute for Zoo and Wildlife Research, p. 197.
32. Anon. (2012) Guidelines for the control of tuberculosis in elephants 2012. In Elephant Tuberculosis Subcommittee (eds.). Saint Joseph, MO, USA: United States Animal Health Association (USAHA), p. 43.
33. EAZA Elephant TAG (2015) TB Testing Recommendation for Elephants. Amsterdam, NL: European Association of Zoo and Aquaria.
34. Greenwald, R, et al. (2009) Highly accurate antibody assays for early and rapid detection of tuberculosis in African and Asian elephants. Clinical and Vaccine Immunology 16: 605612.
35. Vogelnest, L, et al. (2015) Diagnosis and management of tuberculosis (Mycobacterium tuberculosis) in an Asian elephant (Elephas maximus) with a newborn calf. Journal of Zoo and Wildlife Medicine 46, 7785.
36. Angkawanish, T, et al. (2013) The elephant interferon gamma assay: a contribution to diagnosis of tuberculosis in elephants. Transboundry and Emerging Diseases 60, 5359.
37. Sternberg Lewerin, S, et al. (2005) Outbreak of Mycobacterium tuberculosis infection among captive Asian elephants in a Swedish zoo. Veterinary Record 156, 171175.
38. Isaza, R and Ketz, CJ. A trunk wash technique for the diagnosis of tuberculosis in elephants. In Hofmann, RR (ed.). 39th Proceedings of the International Conference on Diseases of Zoo and Wild Animals. Vienna: Leibniz Institute for Zoo and Wildlife Research, 1999, pp. 121124.
39. Moller, T, et al. (2005) Preliminary results of a new serological test for detection of TB-infection (Mycobacterium tuberculosis) in elephants (Elaphas maximus and Loxodonta africanum) Swedish case studies. 42nd Proceedings of the International Conference on Diseases of Zoo and Wild Animals Prague, Leibniz Institute for Zoo and Wildlife Research, pp. 173181.
40. Mikota, SK, et al. (2001) Epidemiology and diagnosis of Mycobacterium tuberculosis in captive Asian elephants (Elephas maximus). Journal of Zoo and Wildlife Medicine 32, 116.
41. Holund, T (1951) [Demonstration of tubercle bacilli in semen.]. Ugeskrift for Laeger 113, 632633.
42. Ladehoff, A (1951) [Tubercle bacilli in semen.]. Ugeskrift for Laeger 113, 834836.
43. Mikota, SK (2008) Review of tuberculosis in captive elephants and implications for wild populations. Gajah 28, 818.
44. Kalawat, U, et al. (2010) Study of bronchoalveolar lavage in clinically and radiologically suspected cases of pulmonary tuberculosis. Lung India 27, 122124.
45. Neiffer, DL, et al. (2005) Standing sedation in African elephants (Loxodonta africana) using detomidine–butorphanol combinations. Journal of Zoo and Wildlife Medicine 36, 250256.
46. Boas, JEV and Paulli, S (1908) The Elephant's Head: Studies in the Comparative Anatomy of the Organs of the Head of the Indian Elephant and Other Mammals: Part I. Copenhagen: Folio, Gustav Fisher.
47. Toussaint, JF, et al. (2007) Bluetongue virus detection by two real-time RT-qPCRs targeting two different genomic segments. Journal of Virological Methods 140, 115123.
48. Anon. (2015). Tuberkulose der Rinder (Mykobakterium bovis und Mykobakterium caprae). In Amtliche Methodensammlung. Jena, Germany: Friedrich-Loeffler-Institut, Bundesforschungsinstitut für Tiergesundheit. Available at https://openagrar.bmel-forschung.de/receive/openagrar_mods_00005698 (Accessed 29 January 2016).
49. Kirschner, P and Böttger, EC (1998) Species identification of mycobacteria using rDNA sequencing. In Parish, T, Stoker, NG (eds). Mycobacteria Protocols. Totowa, NJ: Humana Press, pp. 349361.
50. Guerrero, C, et al. (1995) A novel insertion element from Mycobacterium avium, IS1245, is a specific target for analysis of strain relatedness. Journal of Clinical Microbioloy 33, 304307.
51. Kunze, ZM, Portaels, F and McFadden, JJ (1992) Biologically distinct subtypes of Mycobacterium avium differ in possession of insertion sequence IS901. Journal of Clinical Microbiology 30, 23662372.
52. Moser, I, et al. (2008) Mycobacterium pinnipedii: transmission from South American sea lion (Otaria byronia) to Bactrian camel (Camelus bactrianus bactrianus) and Malayan tapirs (Tapirus indicus). Veterinary Microbiology 127, 399406.
53. Rodriguez, JG, et al. (1995) Species-specific identification of Mycobacterium bovis by PCR. Microbiology 141, 21312138.
54. Oh, P, et al. (2002) Human exposure following Mycobacterium tuberculosis infection of multiple animal species in a metropolitan zoo. Emerging Infectious Diseases 8, 12901293.
55. Maslow, JN and Mikota, SK (2015) Tuberculosis in elephants – a reemergent disease: diagnostic dilemmas, the natural history of infection, and new immunological tools. Veterinary Pathology 52, 437440.
56. Cambau, E and Drancourt, M (2014) Steps towards the discovery of Mycobacterium tuberculosis by Robert Koch, 1882. Clinical Microbiology and Infection 20, 196201.
57. Lueders, I, et al. (2017) A full mouth speculum for elephants facilitating bronchoscopy, gastric tubing, and dental health evaluation. Proceedings Zoo Wildlife Health Conference, Berlin, Germany. Leibniz Institute for Zoo and Wildlife Research, p. 42.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Epidemiology & Infection
  • ISSN: 0950-2688
  • EISSN: 1469-4409
  • URL: /core/journals/epidemiology-and-infection
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

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