Advertisement

Mammalia: Proboscidea: Elephant Immune System

  • Lisa M. Abegglen
  • Angela Fuery
  • Wendy K. Kiso
  • Dennis L. Schmitt
  • Paul D. Ling
  • Joshua D. Schiffman
Chapter

Abstract

Elephant immunology is an emerging field of study. While we still have much to learn about how the elephant immune system differs from the immune systems of other animals and what advantages or disadvantages these differences may provide, our knowledge of the elephant immune system continues to increase as we work to understand disease mechanisms that threaten these incredible animals. Elephant endotheliotropic herpesvirus (EEHV) remains one of the most serious threats to the health and survival of Asian elephants. Immune responses to this virus in elephants are under active investigation in an attempt to understand why some elephants are able to recover, while others rapidly die of progressive disease. The elephant immune responses to EEHV, and other infections in elephants, are a focus of this chapter, which reviews our current understanding of elephant immunology and points to gaps in our knowledge.

Keywords

Elephant Elephant immunology Elephant endotheliotropic herpesvirus EEHV Comparative immunology Bilobed macrophages Comparative oncology Tuberculosis Cancer resistance p53 TP53 

References

  1. Abegglen LM, Caulin AF, Chan A, Lee K, Robinson R, Campbell MS et al (2015) Potential mechanisms for cancer resistance in elephants and comparative cellular response to DNA damage in humans. JAMA 314(17):1850–1860. https://doi.org/10.1001/jama.2015.13134 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Allen JL, Jacobson ER, Harvey JW, Boyce W (1985) Hematologic and serum chemical values for young African elephants (Loxodonta-African) with variations for sex and age. J Zoo Anim Med 16(3):98–101CrossRefGoogle Scholar
  3. Angkawanish T, Wajjwalku W, Sirimalaisuwan A, Mahasawangkul S, Kaewsakhorn T, Boonsri K et al (2010) Mycobacterium tuberculosis infection of domesticated Asian elephants, Thailand. Emerg Infect Dis 16(12):1949–1951PubMedPubMedCentralCrossRefGoogle Scholar
  4. Angkawanish T, Morar D, van Kooten P, Bontekoning I, Schreuder J, Maas M et al (2013) The elephant interferon gamma assay: a contribution to diagnosis of tuberculosis in elephants. Transbound Emerg Dis 60(Suppl 1):53–59PubMedCrossRefGoogle Scholar
  5. Archie EA, Henry T, Maldonado JE, Moss CJ, Poole JH, Pearson VR et al (2010) Major histocompatibility complex variation and evolution at a single, expressed DQA locus in two genera of elephants. Immunogenetics 62(2):85–100PubMedCrossRefGoogle Scholar
  6. Aroch I, King R, Baneth G (2007) Hematology and serum biochemistry values of trapped, healthy, free-ranging rock hyraxes (Procavia capensis) and their association with age, sex, and gestational status. Vet Clin Pathol 36(1):40–48PubMedCrossRefGoogle Scholar
  7. Atkins L, Zong JC, Tan J, Mejia A, Heaggans SY, Nofs SA et al (2013) Elephant endotheliotropic herpesvirus 5, a newly recognized elephant herpesvirus associated with clinical and subclinical infections in captive Asian elephants (Elephas maximus). J Zoo Wildlife Med: Off Publ Am Assoc Zoo Vet. 44(1):136–143CrossRefGoogle Scholar
  8. Berry HH (1993) Surveillance and control of anthrax and rabies in wild herbivores and carnivores in Namibia. Rev Sci Tech 12(1):137–146PubMedCrossRefGoogle Scholar
  9. Birbrair A, Frenette PS (2016) Niche heterogeneity in the bone marrow. Ann N Y Acad Sci 1370(1):82–96PubMedPubMedCentralCrossRefGoogle Scholar
  10. Brown IRF, White PT (1980) Elephant blood hematology and chemistry. Comp Biochem Phys B 65(1):1–12CrossRefGoogle Scholar
  11. Burke TJ (1975) Probable tetanus in an Asian elephant. J Zoo Anim Med 6(1):22–24CrossRefGoogle Scholar
  12. Campbell MS, Lovell MA, Gorbsky GJ (1995) Stability of nuclear segments in human neutrophils and evidence against a role for microfilaments or microtubules in their genesis during differentiation of HL60 myelocytes. J Leukoc Biol 58(6):659–666PubMedCrossRefGoogle Scholar
  13. Caulin AF, Maley CC (2011) Peto’s paradox: evolution’s prescription for cancer prevention. Trends Ecol Evol 26(4):175–182PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cave AJE, Aumonier FJ (1962) Elephant and rhinoceros lymph-node histology. J R Microsc Soc 80(3):209–214CrossRefGoogle Scholar
  15. Chaudhry H, Zhou J, Zhong Y, Ali MM, McGuire F, Nagarkatti PS et al (2013) Role of cytokines as a double-edged sword in sepsis. In Vivo 27(6):669–684PubMedPubMedCentralGoogle Scholar
  16. Chucri TM, Monteiro JM, Lima AR, Salvadori ML, Kfoury JR Jr, Miglino MA (2010) A review of immune transfer by the placenta. J Reprod Immunol 87(1–2):14–20PubMedCrossRefGoogle Scholar
  17. Cizauskas CA, Bellan SE, Turner WC, Vance RE, Getz WM (2014) Frequent and seasonally variable sublethal anthrax infections are accompanied by short-lived immunity in an endemic system. J Anim Ecol 83(5):1078–1090PubMedPubMedCentralCrossRefGoogle Scholar
  18. Clark HW, Laughlin DC, Brown T (eds) (1981) Rheumatoid arthritis in elephants – a review to date. Proc Amer Assoc Zoo Vet, Seattle, WashingtonGoogle Scholar
  19. Cooper RA, Connell RS, Wellings SR (1964) Placenta of the Indian elephant, Elephas Indicus. Science (New York, NY) 146(3642):410–412CrossRefGoogle Scholar
  20. Crapnell K, Zanjani ED, Chaudhuri A, Ascensao JL, St Jeor S, Maciejewski JP (2000) In vitro infection of megakaryocytes and their precursors by human cytomegalovirus. Blood 95(2):487–493PubMedGoogle Scholar
  21. Encyclopedia E. http://www.elephant.se (1995–2017)
  22. Farkona S, Diamandis EP, Blasutig IM (2016) Cancer immunotherapy: the beginning of the end of cancer? BMC Med 14:73PubMedPubMedCentralCrossRefGoogle Scholar
  23. Fermaglich DH, Horohov DW (2002) The effect of aging on immune responses. Vet Clin North Am Equine Pract 18(3):621–630. ixPubMedCrossRefGoogle Scholar
  24. Foley NM, Springer MS, Teeling EC (1699) Mammal madness: is the mammal tree of life not yet resolved? Philos T R Soc B 371:2016Google Scholar
  25. Fuery A, Browning GR, Tan J, Long S, Hayward GS, Cox SK et al (2016a) Clinical infection of captive Asian elephants (Elephas maximus) with elephant Endotheliotropic Herpesvirus 4. J Zoo Wildlife Med : Off Publ Am Assoc Zoo Vet. 47(1):311–318CrossRefGoogle Scholar
  26. Fuery A, Tan J, Peng R, Flanagan J, Tocidlowski ME, Howard LL et al (2016b) Clinical infection of two captive Asian elephants (Elephas Maximus) with elephant Endotheliotropic Herpesvirus 1B. J Zoo Wildlife Med : Off Publ Am Assoc Zoo Vet. 47(1):319–324CrossRefGoogle Scholar
  27. Fuery A, Leen AM, Peng R, Wong MC, Liu H, Ling PD (2018) Asian elephant T cell responses to Elephant Endotheliotropic Herpesvirus. J Virol 92:e01951–01917Google Scholar
  28. Gerna G, Lilleri D, Fornara C, Comolli G, Lozza L, Campana C et al (2006) Monitoring of human cytomegalovirus-specific CD4 and CD8 T-cell immunity in patients receiving solid organ transplantation. Am J Transplant Off J Am Soc Transplant Am Soc Transplant Surg 6(10):2356–2364CrossRefGoogle Scholar
  29. Guleria I, Sayegh MH (2007) Maternal acceptance of the fetus: true human tolerance. J Immunol 178(6):3345–3351PubMedCrossRefGoogle Scholar
  30. Hainz U, Jenewein B, Asch E, Pfeiffer KP, Berger P, Grubeck-Loebenstein B (2005) Insufficient protection for healthy elderly adults by tetanus and TBE vaccines. Vaccine 23(25):3232–3235PubMedCrossRefGoogle Scholar
  31. Hanna P (1998) Anthrax pathogenesis and host response. Curr Top Microbiol Immunol 225:13–35PubMedGoogle Scholar
  32. Hardy RR, Hayakawa K (2001) B cell development pathways. Annu Rev Immunol 19:595–621PubMedCrossRefGoogle Scholar
  33. Harr KEI R, Blue JT (2010) Hematology of elephants. In: Weiss DJ, Wardrop KJ (eds) Schalm's veterinary hematology, 6th edn. Blackwell Publishing Inc, Ames/Iowa, pp 942–949Google Scholar
  34. Heddle RJ, Rowley D (1975) Dog immunoglobulins. I. Immunochemical characterization of dog serum, parotid saliva, colostrum, milk and small bowel fluid. Immunology 29(1):185–195PubMedPubMedCentralGoogle Scholar
  35. Hoffmann K, Sperling K, Olins AL, Olins DE (2007) The granulocyte nucleus and Lamin B receptor: avoiding the ovoid. Chromosoma 116(3):227–235PubMedCrossRefGoogle Scholar
  36. Hou ZC, Sterner KN, Romero R, Than NG, Gonzalez JM, Weckle A et al (2012) Elephant Transcriptome provides insights into the evolution of Eutherian placentation. Genome Biol Evol 4(5):713–725PubMedPubMedCentralCrossRefGoogle Scholar
  37. Humphreys AF, Tan J, Peng R, Benton SM, Qin X, Worley KC et al (2015) Generation and characterization of antibodies against Asian elephant (Elephas maximus) IgG, IgM, and IgA. PLoS One 10(2):e0116318PubMedPubMedCentralCrossRefGoogle Scholar
  38. Isaza R, Davis RD, Moore SM, Briggs DJ (2006) Results of vaccination of Asian elephants (Elephas maximus) with monovalent inactivated rabies vaccine. Am J Vet Res 67(11):1934–1936PubMedCrossRefGoogle Scholar
  39. Jacobson ER, Sundberg JP, Gaskin JM, Kollias GV, O'Banion MK (1986) Cutaneous papillomas associated with a herpesvirus-like infection in a herd of captive African elephants. J Am Vet Med Assoc 189(9):1075–1078PubMedGoogle Scholar
  40. Janeway CA Jr, Travers P, Walport M, Shlomchik MJ (2001) The major histocompatibility complex and its functions. In: Immunobiology, 5th edn. Garland Science, New YorkGoogle Scholar
  41. Janssen DL, Karesh WB, Cosgrove GE, Oosterhuis JE (1984) Salmonellosis in a herd of captive elephants. J Am Vet Med Assoc 185(11):1450–1451PubMedGoogle Scholar
  42. Janssen LME, Ramsay EE, Logsdon CD, Overwijk WW (2017) The immune system in cancer metastasis: friend or foe? J Immunother Cancer 5(1):79PubMedPubMedCentralCrossRefGoogle Scholar
  43. Jasenosky LD, Scriba TJ, Hanekom WA, Goldfeld AE (2015) T cells and adaptive immunity to mycobacterium tuberculosis in humans. Immunol Rev 264(1):74–87PubMedCrossRefGoogle Scholar
  44. Kastenhuber ER, Lowe SW (2017) Putting p53 in context. Cell 170(6):1062–1078PubMedCrossRefGoogle Scholar
  45. Kelly PJ, Carter SD, Azwai SM, Cadman HF (1998) Isolation and characterisation of immunoglobulin g and IgG subclasses of the African elephant (Loxodonta africana). Comp Immunol Microbiol Infect Dis 21(1):65–73PubMedCrossRefGoogle Scholar
  46. Kelso A (1998) Cytokines: principles and prospects. Immunol Cell Biol 76(4):300–317PubMedCrossRefGoogle Scholar
  47. Landolfi JA, Schultz SA, Mikota SK, Terio KA (2009) Development and validation of cytokine quantitative, real time RT-PCR assays for characterization of Asian elephant immune responses. Vet Immunol Immunopathol 131(1–2):73–78PubMedCrossRefGoogle Scholar
  48. Landolfi JA, Mikota SK, Chosy J, Lyashchenko KP, Giri K, Gairhe K et al (2010) Comparison of systemic cytokine levels in mycobacterium spp. seropositive and seronegative Asian elephants (Elephas maximus). J Zoo Wildl Med 41(3):445–455PubMedCrossRefGoogle Scholar
  49. Landolfi JA, Miller M, Maddox C, Zuckermann F, Langan JN, Terio KA (2014) Differences in immune cell function between tuberculosis positive and negative Asian elephants. Tuberculosis (Edinb) 94(4):374–382CrossRefGoogle Scholar
  50. Landolfi JA, Terio KA, Miller M, Junecko BF, Reinhart T (2015) Pulmonary tuberculosis in Asian elephants (Elephas maximus): histologic lesions with correlation to local immune responses. Vet Pathol 52(3):535–542PubMedCrossRefGoogle Scholar
  51. Lewerin SS, Olsson SL, Eld K, Roken B, Ghebremichael S, Koivula T et al (2005) Outbreak of mycobacterium tuberculosis infection among captive Asian elephants in a Swedish zoo. Vet Rec 156(6):171–175PubMedCrossRefGoogle Scholar
  52. Lindeque PM, Turnbull PC (1994) Ecology and epidemiology of anthrax in the Etosha National Park, Namibia. Onderstepoort J Vet Res 61(1):71–83PubMedGoogle Scholar
  53. Lindsay WA, Wiedner E, Isaza R, Townsend HG, Boleslawski M, Lunn DP (2010) Immune responses of Asian elephants (Elephas maximus) to commercial tetanus toxoid vaccine. Vet Immunol Immunopathol 133(2–4):287–289PubMedCrossRefGoogle Scholar
  54. Liu CH, Chang CH, Chin SC, Chang PH, Zhuo YX, Lee CC (2004) Fibrosarcoma with lung and lymph node metastases in an Asian elephant (Elephas maximus). J Vet Diagn Investig 16(5):421–423CrossRefGoogle Scholar
  55. Long SY, Latimer EM, Hayward GS (2016) Review of elephant endotheliotropic herpesviruses and acute hemorrhagic disease. ILAR J/Nat Res Counc Inst Lab Anim Res 56(3):283–296Google Scholar
  56. Lowenstine LJ (2006) Endocrine and immune systems. In: Fowler ME, Mikota SK (eds) Biology, medicine, and surgery of elephants. Blackwell Publishing, Oxford, pp 309–315CrossRefGoogle Scholar
  57. Lukasova E, Koristek Z, Klabusay M, Ondrej V, Grigoryev S, Bacikova A et al (2013) Granulocyte maturation determines ability to release chromatin NETs and loss of DNA damage response; these properties are absent in immature AML granulocytes. Biochim Biophys Acta 1833(3):767–779PubMedCrossRefGoogle Scholar
  58. Marcus H, Danieli R, Epstein E, Velan B, Shafferman A, Reuveny S (2004) Contribution of immunological memory to protective immunity conferred by a bacillus anthracis protective antigen-based vaccine. Infect Immun 72(6):3471–3477PubMedPubMedCentralCrossRefGoogle Scholar
  59. Maslow JN, Mikota SK (2015) Tuberculosis in elephants-a reemergent disease: diagnostic dilemmas, the natural history of infection, and new immunological tools. Vet Pathol 52(3):437–440PubMedCrossRefGoogle Scholar
  60. McBride KA, Ballinger ML, Killick E, Kirk J, Tattersall MH, Eeles RA et al (2014) Li-Fraumeni syndrome: cancer risk assessment and clinical management. Nat Rev Clin Oncol 11(5):260–271PubMedCrossRefGoogle Scholar
  61. McCully RM, Basson PA, Pienaar JG, Erasmus BJ, Young E (1971) Herpes nodules in the lung of the African elephant (Loxodonta africana (Blumebach, 1792)). Onderstepoort J Vet Res 38(4):225–235PubMedGoogle Scholar
  62. McGee JL, Wiedner E, Isaza R (2014) Prenatal passive transfer of mycobacterium tuberculosis antibodies in Asian elephant (Elephas maximus) calves. J Zoo and Wildlife Med : Off Publ Am Assoc Zoo Vet 45(4):955–957CrossRefGoogle Scholar
  63. Metzler AE, Ossent P, Guscetti F, Rubel A, Lang EM (1990) Serological evidence of herpesvirus infection in captive Asian elephants (Elephas maximus). J Wildl Dis 26(1):41–49PubMedCrossRefGoogle Scholar
  64. Meyer H, Schay C, Mahnel H, Pfeffer M (1999) Characterization of orthopoxviruses isolated from man and animals in Germany. Arch Virol 144(3):491–501PubMedCrossRefGoogle Scholar
  65. Mikota SK (2006) Hemolymphatic system. In: Fowler ME, Mikota SK (eds) Biology, medicine, and surgery of elephants. Blackwell Publishing, Oxford, pp 325–345CrossRefGoogle Scholar
  66. Mikota SK, Maslow JN (2011) Tuberculosis at the human-animal interface: an emerging disease of elephants. Tuberculosis (Edinb) 91(3):208–211CrossRefGoogle Scholar
  67. Miller MA, Olea-Popelka F (2009) Serum antibody titers following routine rabies vaccination in African elephants. J Am Vet Med Assoc 235(8):978–981PubMedCrossRefGoogle Scholar
  68. Muirhead TL, McClure JT, Wichtel JJ, Stryhn H, Frederick Markham RJ, McFarlane D et al (2008) The effect of age on serum antibody titers after rabies and influenza vaccination in healthy horses. J Vet Intern Med 22(3):654–661PubMedCrossRefGoogle Scholar
  69. Nganvongpanit K, Siengdee P, Buddhachat K, Brown JL, Klinhom S, Pitakarnnop T et al (2017) Anatomy, histology and elemental profile of long bones and ribs of the Asian elephant (Elephas maximus). Anat Sci Int 92(4):554–568PubMedCrossRefGoogle Scholar
  70. Nofs SA, Atmar RL, Keitel WA, Hanlon C, Stanton JJ, Tan J et al (2013) Prenatal passive transfer of maternal immunity in Asian elephants (Elephas maximus). Vet Immunol Immunopathol 153(3–4):308–311PubMedCrossRefGoogle Scholar
  71. Olins AL, Zwerger M, Herrmann H, Zentgraf H, Simon AJ, Monestier M et al (2008) The human granulocyte nucleus: unusual nuclear envelope and heterochromatin composition. Eur J Cell Biol 87(5):279–290PubMedPubMedCentralCrossRefGoogle Scholar
  72. Ossent P, Guscetti F, Metzler AE, Lang EM, Rubel A, Hauser B (1990) Acute and fatal herpesvirus infection in a young Asian elephant (Elephas maximus). Vet Pathol 27(2):131–133PubMedCrossRefGoogle Scholar
  73. Pearse G (2006) Normal structure, function and histology of the thymus. Toxicol Pathol 34(5):504–514PubMedCrossRefGoogle Scholar
  74. Perry JS (1974) Implantation, foetal membranes and early placentation of the African elephant, Loxodonta africana. Philos Trans R Soc Lond Ser B Biol Sci 269(897):109–135CrossRefGoogle Scholar
  75. Pilaski J, Rosen A, Darai G (1986) Comparative analysis of the genomes of orthopoxviruses isolated from elephant, rhinoceros, and okapi by restriction enzymes. Brief report. Arch Virol 88(1–2):135–142PubMedCrossRefGoogle Scholar
  76. Prescott JB, Marzi A, Safronetz D, Robertson SJ, Feldmann H, Best SM (2017) Immunobiology of Ebola and Lassa virus infections. Nat Rev Immunol 17(3):195–207PubMedCrossRefGoogle Scholar
  77. Reuveny S, White MD, Adar YY, Kafri Y, Altboum Z, Gozes Y et al (2001) Search for correlates of protective immunity conferred by anthrax vaccine. Infect Immun 69(5):2888–2893PubMedPubMedCentralCrossRefGoogle Scholar
  78. Richman LK, Montali RJ, Garber RL, Kennedy MA, Lehnhardt J, Hildebrandt T et al (1999) Novel endotheliotropic herpesviruses fatal for Asian and African elephants. Science (New York, NY) 283(5405):1171–1176CrossRefGoogle Scholar
  79. Richman LK, Montali RJ, Cambre RC, Schmitt D, Hardy D, Hildbrandt T et al (2000) Clinical and pathological findings of a newly recognized disease of elephants caused by endotheliotropic herpesviruses. J Wildl Dis 36(1):1–12PubMedCrossRefGoogle Scholar
  80. Richman LK, Zong JC, Latimer EM, Lock J, Fleischer RC, Heaggans SY et al (2014) Elephant endotheliotropic herpesviruses EEHV1A, EEHV1B, and EEHV2 from cases of hemorrhagic disease are highly diverged from other mammalian herpesviruses and may form a new subfamily. J Virol 88(23):13523–13546PubMedPubMedCentralCrossRefGoogle Scholar
  81. Sester M, Sester U, Gartner B, Heine G, Girndt M, Mueller-Lantzsch N et al (2001) Levels of virus-specific CD4 T cells correlate with cytomegalovirus control and predict virus-induced disease after renal transplantation. Transplantation 71(9):1287–1294PubMedCrossRefGoogle Scholar
  82. Silva ID, Kuruwita VY (1993) Hematology, plasma, and serum biochemistry values in free-ranging elephants (Elephas-Maximus Ceylonicus) in Sri-Lanka. J Zoo Wildlife Med 24(4):434–439Google Scholar
  83. Simon KJ (1961) Haematological studies on elephants. Indian Vet J 38:241Google Scholar
  84. Sin JI, Kim JJ, Boyer JD, Ciccarelli RB, Higgins TJ, Weiner DB (1999) In vivo modulation of vaccine-induced immune responses toward a Th1 phenotype increases potency and vaccine effectiveness in a herpes simplex virus type 2 mouse model. J Virol 73(1):501–509PubMedPubMedCentralGoogle Scholar
  85. Stacy NI, Isaza R, Wiedner E (2017) First report of changes in leukocyte morphology in response to inflammatory conditions in Asian and African elephants (Elephas maximus and Loxodonta africana). PLoS One 12(9):e0185277PubMedPubMedCentralCrossRefGoogle Scholar
  86. Stanhope MJ, Madsen O, Waddell VG, Cleven GC, de Jong WW, Springer MS (1998) Highly congruent molecular support for a diverse superordinal clade of endemic African mammals. Mol Phylogenet Evol 9(3):501–508PubMedCrossRefGoogle Scholar
  87. Stephens N, Vogelnest L, Lowbridge C, Christensen A, Marks GB, Sintchenko V et al (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(7):1488–1497PubMedCrossRefGoogle Scholar
  88. Tisoncik JR, Korth MJ, Simmons CP, Farrar J, Martin TR, Katze MG (2012) Into the eye of the cytokine storm. Microbiol Mol Biol Rev : MMBR 76(1):16–32PubMedCrossRefGoogle Scholar
  89. Turnbull PC, Bell RH, Saigawa K, Munyenyembe FE, Mulenga CK, Makala LH (1991) Anthrax in wildlife in the Luangwa Valley, Zambia. Vet Rec 128(17):399–403PubMedCrossRefGoogle Scholar
  90. Valli VE, Jacobs RM (2000) Structure and function of the hemopoietic system. In: Feldman BF, Zinkl JG, Jain NC, Schalm OW (eds) Schalm’s veterinary hematology. Lippincott, Williams & Wilkins, Philadelphia, pp 225–239Google Scholar
  91. van der Kolk JH, Hoyer MJ, Verstappen FA, Wolters MS, Treskes M, Grinwis GC et al (2011) Diabetes mellitus in a 50-year-old captive Asian elephant (Elaphas maximus) bull. Vet Q 31(2):99–101PubMedCrossRefGoogle Scholar
  92. Viret C, Janeway CA Jr (1999) MHC and T cell development. Rev Immunogenet 1(1):91–104PubMedGoogle Scholar
  93. Wang FZ, Linde A, Dahl H, Ljungman P (1999) Human herpesvirus 6 infection inhibits specific lymphocyte proliferation responses and is related to lymphocytopenia after allogeneic stem cell transplantation. Bone Marrow Transplant 24(11):1201–1206PubMedCrossRefGoogle Scholar
  94. Weinberg A, Levin MJ (2010) VZV T cell-mediated immunity. Curr Top Microbiol Immunol 342:341–357PubMedGoogle Scholar
  95. Wimalaratne O, Kodikara DS (1999) First reported case of elephant rabies in Sri Lanka. Vet Rec 144(4):98PubMedCrossRefGoogle Scholar
  96. Wisser J, Pilaski J, Strauss G, Meyer H, Burck G, Truyen U et al (2001) Cowpox virus infection causing stillbirth in an Asian elephant (Elphas maximus). Vet Rec 149(8):244–246PubMedCrossRefGoogle Scholar
  97. Woodford MH, Keet DF, Bengis RG (2000) A guide to post-mortem procedure and a review of pathological processes identified in the elephant. In: Woodford MH (ed) Post-mortem procedures for wildlife veterinarians and field biologists. Office International des Epizooties, Care for the Wild and the Vererinary Specialist Group/Species Survival Commission of the World Conservation Union (IUCN), France, pp 36–47Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Lisa M. Abegglen
    • 1
  • Angela Fuery
    • 2
  • Wendy K. Kiso
    • 3
  • Dennis L. Schmitt
    • 3
  • Paul D. Ling
    • 2
  • Joshua D. Schiffman
    • 4
  1. 1.Department of PediatricsUniversity of UtahSalt Lake CityUSA
  2. 2.Molecular Virology and MicrobiologyBaylor College of MedicineHoustonUSA
  3. 3.Ringling Bros. Center for Elephant ConservationPolk CityUSA
  4. 4.Departments of Pediatrics and Oncological SciencesUniversity of UtahSalt Lake CityUSA

Personalised recommendations