Advertisement

Serodiagnosis of elephant tuberculosis: a useful tool for early identification of infected elephants at the captive-wild interface

  • Sarad Paudel
  • Susan K. Mikota
  • Jeewan Thapa
  • Konstantin P. Lyashchenko
  • Kamal P. Gairhe
  • Ishwari Prasad Dhakal
  • Naresh Subedi
  • Bhagwan Maharjan
  • Suraj Subedi
  • Gretchen E. Kaufman
  • Toshio TsubotaEmail author
Short Communication

Abstract

Tuberculosis (TB) is an emerging disease in elephants primarily caused by Mycobacterium tuberculosis (M. tb) and in some occassion by M. bovis. We performed culture and three serological tests—the Elephant TB STAT-PAK,® DPP VetTB® Assay, and MAPIA (multi-antigen print immunoassay)—prospectively on samples from eight elephants in Nepal that died of suspected or confirmed tuberculosis (TB) between 2007 and 2013. Among them, all elephants were reactive to DPP VetTB® Assay, five to Elephant TB STAT-PAK,® and two were reactive to MAPIA. Similarly, six elephants were positive on culture on samples collected antemortem or postmortem. We observed antibody responses months to years before culture confirmation of TB which shows that serological tests can be highly useful for the early diagnosis of TB in elephants. Validated point-of-care serological tests are easily performed in the field and hold promise for improved TB surveillance in other non-domestic species.

Keywords

Asian elephants Tuberculosis DPP VetTB assay ElephantTB STAT-PAK Serological assay 

Notes

Acknowledgments

We acknowledge Chitra Bahadur Khadka, Purushottam Pandey, and Kiran Rijal at Chitwan National Park, Nepal for helping with blood collection and sample collection during the necropsy. We highly acknowledge the Department of National Parks and Wildlife Conservation (DNPWC), Government of Nepal, National Trust of Nature Conservation (NTNC), Nepal, and WWF-Nepal for their kind support in this study.

Funding information

This elephant TB study in Nepal is funded by Christy Williams, Asian Rhino and Elephant Action Strategy (AREAS), and WWF-Nepal.

Supplementary material

10344_2018_1229_MOESM1_ESM.docx (69 kb)
ESM 1 (DOCX 69.2 kb)

References

  1. Abraham D, Davis J (2008) Revised trunk wash collection procedure for captive elephants in a range country setting. Gajah 28:53–54Google Scholar
  2. Abraham D, Cheeran JV, Sukumar R, Mikota SK, Rao S, Ganguly S, Varma S (2008) 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 DelhiGoogle Scholar
  3. Angkawanish T, Wajjwalku W, Sirimalaisuwan A, Mahasawangkul S, Kaewsakhorn T, Boonsri K, Rutten VP (2010) Mycobacterium tuberculosis infection of domesticated Asian elephants, Thailand. Emerg Infect Dis 16:1949–1951CrossRefGoogle Scholar
  4. Chandranaik BM, Shivashankar BP, Umashankar KS, Nandini P, Giridhar P, Byregowda SM, Shrinivasa BM (2017) Mycobacterium tuberculosis infection in free-roaming wild Asian elephant. Emerg Infect Dis 23:555–557CrossRefGoogle Scholar
  5. Drewe JA, Tomlinson AJ, Walker NJ, Delahay RJ (2010) Diagnostic accuracy and optimal use of three tests for tuberculosis in live badgers. PLoS One 5(6):e11196.  https://doi.org/10.1371/journal.pone.0011196 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Duncan AE, Lyashchenko K, Greenwald R, Miller M, Ball R (2009) Application of elephant TB STAT-PAK assay and MAPIA (multi-antigen print immunoassay) for detection of tuberculosis and monitoring of treatment in black rhinoceros (Diceros bicornis). J Zoo Wildl Med 40(4):781–785CrossRefGoogle Scholar
  7. Greenwald R, Lyashchenko O, Esfandiari J, Miller M, Mikota S, Olsen JH, Ball R, Dumonceaux G, Schmitt D, Moller T, Payeur JB, Harris B, Sofranko D, Waters WR, Lyashchenko KP (2009) Highly accurate antibody assays for early and rapid detection of tuberculosis in African and Asian elephants. Clin Vaccine Immunol 16:605–612CrossRefGoogle Scholar
  8. Groothuis DG, Yates MD (1991) Decontamination, microscopy and isolation. In: Groothius DG, Yates MD (eds) Diagnostic and Public Health Mycobacteriology, 2nd edn. Bureau of Hygiene and Tropical Diseases, European Society for Mycobacteriology, London, p 63Google Scholar
  9. Himsworth CG, Elkin BT, Nishi JS, Epp T, Lyashchenko KP, Surujballi O, Turcotte C, Esfandiari J, Greenwald R, Leighton FA (2010) Comparison of test performance and evaluation of novel immunoassays for tuberculosis in a captive herd of wood bison naturally infected with Mycobacterium bovis. J Wild Dis 46(1):78–86CrossRefGoogle Scholar
  10. Lassausaie J, Bret A, Bouapao X, Chanthavong V, Castonguay-Vanier J, Quet F, Mikota SK, Théorêt C, Buisson Y, Bouchard B (2015) Tuberculosis in Laos, who is at risk: the mahouts or their elephants? Epidemiol Infect 143:922–931CrossRefGoogle Scholar
  11. 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 D, Waters WR (2006) Tuberculosis in elephants: antibody responses to defined antigens of Mycobacterium tuberculosis, potential for early diagnosis, and monitoring of treatment. Clin Vaccine Immunol 13:722–732CrossRefGoogle Scholar
  12. Lyashchenko KP, Greenwald R, Esfandiari J, Mikota S, Miller M, Moller T, Volgelnest L, Gairhe K, Robbe-Austerman S, Gai J, Waters WR (2012) Field application of serodiagnostics to identify elephants with tuberculosis prior to case confirmation by culture. Clin Vaccine Immunol 19:1269–1275CrossRefGoogle Scholar
  13. Lyashchenko KP, Greenwald R, Esfandiari J, O'Brien DJ, Schmitt SM, Palmer MV, Waters WR (2013) Rapid detection of serum antibody by dual-path platform VetTB assay in white-tailed deer infected with Mycobacterium bovis. ClinVaccine Immunol 20:907–911Google Scholar
  14. Lyashchenko KP, Gortazar C, Miller MA, Waters WR (2018) Spectrum of antibody profiles in tuberculous elephants, cervids, and cattle. Vet Microbiol 214:89–92CrossRefGoogle Scholar
  15. Mar KU, Htut W, Zar MN, Soe AT, Mikota SK (2012) Report to Myanma Timber Enterprise on Tuberculosis Testing of MTE ElephantsGoogle Scholar
  16. Mikota SK (2008) Tuberculosis in elephants. In: Fowler ME, Miller RE (eds) Zoo and wild animal medicine, current therapy, 6th edn. Saunders/Elsevier, St. Louis, pp 355–364CrossRefGoogle Scholar
  17. Mikota SK, Lyashchenko KP, Lowenstine L, Agnew D, Maslow JN (2015) Mycobacterial infections in elephants. In: Mukundan H, Chambers MA, Waters WR, Larsen M (eds) Many hosts of mycobacteria, tuberculosis, leprosy, and other mycobacterial diseases of man and animals. CABI Publishing House, Wallingford, pp 259–276CrossRefGoogle Scholar
  18. Mikota SK, Kaufman GE, Subedi N, Dhakal IP (2016) Mycobacterium tuberculosis in elephants in Asia - taking a one health approach. In: Cork S, Hall DC, Liljebjelke (eds) One health case studies: addressing complex problems in a changing world. 5M Publishing Ltd, Sheffield, pp 54–64Google Scholar
  19. Miller M, Joubert J, Mathebula N, de-Klerk-Lorist LM, Lyashchenko KP, Bengis R, van Helden P, Hofmeyr M, Olea-Popelka F, Greenwald R, Esfandiari J, Buss P (2012) Detection of antibodies to tuberculosis antigens in free-ranging lions (panthera leo) infected withmycobacterium bovisin kruger national park, South Africa. J Zoo Wild Med 43(2):317–323CrossRefGoogle Scholar
  20. Miller MA, Greenwald R, Lyashchenko KP (2015) Potential for serodiagnosis of tuberculosis in black rhinoceros (Diceros bicornis). J Zoo Wild Med 46(1):100–104CrossRefGoogle Scholar
  21. Miller M, Buss P, de-Klerk-Lorist LM, Hofmeyr J, Hausler G, Lyashchenko K, Lane EP, Botha L, Parsons S, van Helden P (2016) Application of rapid serologic tests for detection of Mycobacterium bovis infection in free-ranging warthogs (Phacochoerus africanus) — implications for antemortem disease screening. J Wild Dis 52(1):180–182CrossRefGoogle Scholar
  22. Moller T, Roken B, Petersson L, Vitaud C, Lyashchenko K (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. Verh ber Erkg Zootiere 42:173e81Google Scholar
  23. Montali RJ (2006) Postmortem diagnostics. In: Fowler M, Mikota SK (eds) Biology, medicine, and surgery of elephants. Blackwell publishing, Ames, pp 199–209CrossRefGoogle Scholar
  24. Obanda VJ, Poghon M, Yongo M, Mulei I, Ngotho K, Waititu K, Makumi J, Gakuya F, Osmondi P, Soriguer RC, Alasaad S (2013) First reported case of fatal tuberculosis in a wild African elephant with past human-wildlife contact. Epidemiol Infect 141:1476–1480CrossRefGoogle Scholar
  25. Ong BL, Ngeow YF, Razak MF, Yakubu Y, Zakaria Z, Mutalib AR, Hassan L, Ng HF, Verasahib K (2013) Tuberculosis in captive Asian elephants (Elephas maximus) in peninsular Malaysia. Epidemiol Infect 141:1481–1487CrossRefGoogle Scholar
  26. Paudel S, Mikota SK, Nakajima C, Gairhe KP, Maharjan B, Thapa J, Poudel A, Shimozuru M, Suzuki Y, Tsubota T (2014) Molecular characterization of Mycobacterium tuberculosis isolates from elephants of Nepal. Tuberculosis 94:287–292CrossRefGoogle Scholar
  27. Perera BVP, Salgadu MA, Gunawardena GSPS, Smith NH, Jinadasa HRN (2014) First confirmed case of fatal tuberculosis in a wild Sri Lankan elephant. Gajah 41:28–31Google Scholar
  28. Pradhan NMB, Williams CA, Dhakal M (2011) Current status of Asian elephants in Nepal. Gajah 35:87–92Google Scholar
  29. Stephens N, Vogelnest L, Lowbridge C, Christensen A, Marks GB, Sintchenko V, McAnulty J (2013) Transmission of Mycobacterium tuberculosis from an Asian elephant (Elephas maximus) to a chimpanzee (Pan troglodytes) and humans in an Australian zoo. Epidemiol Infect 141:1488–1497CrossRefGoogle Scholar
  30. USAHA Proceedings (2010) Guidelines for the control of tuberculosis in elephants. In: Proceedings of 114th Annual Meeting of the United States Animal Health Association, vol 114, p 578–639Google Scholar
  31. Venugopal, K.P., Abraham, D. (2015) Zoonotic tuberculosis: the case of mahouts and captive elephants in southern India, poster presentation, the 46th union world congress on lung health, international union against tuberculosis and lung Diseases, 2–6 December, Cape Town, South AfricaGoogle Scholar
  32. Zachariah A, Pandiyan J, Madhavilatha GK, Mundayoor S, Chandramohan B, Sajesh PK, Santhosh S, Mikota SK (2017) Mycobacterium tuberculosis in wild Asian elephants, southern India. Emerg Infect Dis 23:504–506CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Sarad Paudel
    • 1
    • 2
  • Susan K. Mikota
    • 3
  • Jeewan Thapa
    • 4
  • Konstantin P. Lyashchenko
    • 5
  • Kamal P. Gairhe
    • 6
  • Ishwari Prasad Dhakal
    • 7
  • Naresh Subedi
    • 8
  • Bhagwan Maharjan
    • 9
  • Suraj Subedi
    • 8
  • Gretchen E. Kaufman
    • 10
  • Toshio Tsubota
    • 1
    Email author
  1. 1.Laboratory of Wildlife Biology and Medicine, Graduate School of Veterinary MedicineHokkaido UniversitySapporoJapan
  2. 2.Department of Cell Physiology, Faculty of Medicine and Graduate School of MedicineHokkaido UniversitySapporoJapan
  3. 3.Elephant Care InternationalHohenwaldUSA
  4. 4.Hokkaido University Research Center for Zoonosis ControlSapporoJapan
  5. 5.Chembio Diagnostic Systems, Inc.MedfordUSA
  6. 6.Department of National Parks and Wildlife ConservationChitwan National ParkChitwanNepal
  7. 7.Agriculture and Forestry UniversityRampurNepal
  8. 8.National Trust for Nature ConservationLalitpurNepal
  9. 9.German Nepal Tuberculosis Project (GENETUP)KathmanduNepal
  10. 10.Veterinary Initiative for Endangered WildlifeBozemanUSA

Personalised recommendations