Elephant endotheliotropic herpesvirus

Last updated
Elephantid betaherpesvirus 1
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Duplodnaviria
Kingdom: Heunggongvirae
Phylum: Peploviricota
Class: Herviviricetes
Order: Herpesvirales
Family: Orthoherpesviridae
Genus: Proboscivirus
Species:
Elephantid betaherpesvirus 1
Synonyms [1]

Elephantid herpesvirus 1

Elephant endotheliotropic herpesviruses (EEHV) or Elephantid betaherpesvirus 1 (ElHV-1) is a type of herpesvirus, which can cause a highly fatal hemorrhagic disease when transmitted to young Asian elephants. In African elephants, related forms of these viruses, which have been identified in wild populations, are generally benign, occasionally surfacing to cause small growths or lesions. However, some types of EEHV can cause a highly fatal disease in Asian elephants, which kills up to 80% of severely affected individuals. The disease can be treated with the rapid application of antiviral drugs, but this has only been effective in around a third of cases.

Contents

The first case of a fatal form of the disease was documented in 1990, [2] though tissue samples from as early as the 1980s have since tested positive for the virus, and localized skin lesions in wild African elephants were recorded in the 1970s. Since 1995, there have been over fifty documented disease cases in North America and Europe, of which only nine have been successfully cured. Those affected are mostly young animals born in captivity, though a small number of older wild-born adults held in zoos have died, and a number of cases caused by the same pathogenic type of EEHV have been identified in both orphan and wild calves in Asian elephant populations.

Virus and transmission

"Donaldson", a male Asian elephant calf at Whipsnade Zoo, died of EEHV in May 2009. Baby Elephant.jpg
"Donaldson", a male Asian elephant calf at Whipsnade Zoo, died of EEHV in May 2009.

The EEHVs are members of the Proboscivirus genus, a novel clade most closely related to the mammalian betaherpesviruses that have been responsible for as many as 70 deaths of both zoo and wild Asian elephants worldwide, especially in young calves. [4] [5] There are currently six known species/types of the probosciviruses, and the most commonly encountered and most pathogenic form EEHV1 also has two chimeric subtypes, 1A and 1B, [4] [6] [7] [8] [9] as well as numerous distinct strains. [10]

EEHV1A (originally just known as EEHV1) was the first species/type identified, which causes an acute hemorrhagic disease with a very high mortality rate in Asian elephants. [7] [11] [12] This form of the virus was originally believed to occur naturally in African elephants (occasionally producing skin nodules), and to be transmitted to Asian elephants within captivity, but more extensive studies have since largely disproved this concept because several other species/types of EEHV (e.g. EEHV2, EEHV3 and EEHV6) instead have been identified in African elephants. [5] [13] A second lethal subtype, EEHV1B, was identified in Asian elephants in 2001. [7] EEHV3, EEHV4 and EEHV5 have also each been responsible for the deaths of at least one Asian elephant calf. [14] [15]

EEHV2 has caused hemorrhagic disease in several African elephants as reported by. [9] [11] Along with EEHV3 and EEHV6 it has also been found in pulmonary lymph nodes of several autopsied wild and zoo African elephants. [4] [16]

There are a further five or six species/types and varieties of elephant gammaherpesvirus (EGHVs) found in eye and genital secretions of many healthy Asian and African zoo elephants - e.g. EGHV1, EGHV2, EGHV3A, EGHV3B, EGHV4 and EGHV5 (also called Elephantid gammaherpesviruses EIHV3, EIHV4, EIHV5, EIHV6, ElHV9 and ElHV10) - all of which are classified in the subfamily Gammaherpesvirinae rather than Betaherpesvirinae. These viruses are neither closely related to the EEHVs, nor the known cause of any disease symptoms. [5] [17]

Studies have also detected both EEHV1A and EEHV1B as being shed in trunk wash secretions by healthy asymptomatic Asian zoo elephant herdmates of calves that previously had disease. [18] [19] and similarly for EEHV5. [20] Thus, similar to saliva for most human and animal herpesviruses, the trunk secretions may be a source of transmission for EEHVs. Because of concerns about the origins of EEHV1 and evidence of cross-species transmission for EEHV3, long-term contact between Asian and African elephants has been discouraged, [8] along with avoiding new contacts between young captive-born Asian elephants and wild-born Asian elephants, as the latter may be carriers of the disease. [4] An analysis of a number of North American cases, which ruled out the direct transmission of the virus between any of the affected facilities studied, strongly supported the idea of a significant Asian carrier population. [4] This is supported by the fact that some of the deceased calves had no possible contact with any African elephants. [8] Artificial insemination is not believed to be a transmission factor, [4] notes that when multiple calves of a single bull or cow elephant died at different times (even at the same facility) they nearly all had distinct strains of the virus, yet when two calves died or became infected at the same time at the same facility the pairs have always had identical virus strains. [21] A program of enzyme-linked immunosorbent assay testing began in 2005, aiming to test blood samples from around a thousand elephants for antibodies to the virus in order to help identify carriers and possible transmission patterns. [21]

Effects and treatment

In benign infections found in some wild and captive African elephants, these viruses can affect either the skin or the pulmonary system. [8] In the former case, it produces small pinkish nodules on the head and trunk in juveniles, which appear for a few weeks and then regress, suggesting an intermittently reactivated localized infection that mostly remains dormant. [4] In the second case, it has been found in small white pulmonary nodules on necropsy of many asymptomatic adults. These are both characteristic of EEHV2, EEHV3 and EEHV6. [4]

In a fatal attack, however, it manifests very quickly. In a number of cases, death has occurred within 24 hours of the onset of the infection, [4] while other cases do not last longer than around five days. [8] The virus attacks endothelial cells, rupturing capillaries and causing blood loss and haemorrhaging; once this reaches the heart, the haemorrhage kills quickly through shock. Symptoms include lethargy and an unwillingness to eat, a rapid heartbeat, and decreased blood-cell count, as well as cyanosis of the tongue, mouth ulcers, and oedema of the head and trunk. [8]

Rapid treatment with famciclovir, sustained for around a month, has appeared to cure eight calves infected with EEHV1; however, this treatment is very expensive, only partially effective, and relies on early identification of the infection. [4]

A polymerase chain reaction test on a blood sample from affected animals will confirm a suspected case by identifying the viral DNA, though it is now common to start famciclovir treatment at the earliest possible moment rather than waiting for confirmation of the case. [4] [21] Prior to the development of the test, or in circumstances where it is not available, the disease may be misdiagnosed as any of a number of other conditions which have a quick onset leading to rapid death, including encephalomyocarditis and salmonellosis. [8]

History

The virus has been identified in the pulmonary nodules of African elephants as far back as the 1970s. [8] The first recognised fatal case of EEHV in an Asian elephant was identified at the National Zoo in Washington, D.C., in 1995; [22] testing on stored tissue samples was able to identify a number of earlier deaths as being due to the same virus. These cases have so far been identified as early as 1983. [4] Since this date, there have been a total of 54 more cases in North America and Europe, nine of which were successfully treated. [4] The May 2009 deaths of two calves at Whipsnade Zoo were not included in this calculation. This gives a fatality rate of over 80% among known symptomatic disease cases. In cases where antiviral medication was applied, treatment was effective in about one in three cases. As of 2005, there were twelve cases where famciclovir had been used, eight of which were fatal. As a fraction of the overall population, it has been calculated that of the 78 Asian elephants born in captivity in North America between 1978 and 2007, 19 are known to have died of EEHV, and five more were successfully treated with antiviral medication. [4] [6]

The affected animals are mostly young Asian elephants that had been born in captivity, with half the cases in North America being between the ages of one and four years (and three-quarters between one and eight years old). Some cases have affected newborns or adult elephants born in the wild (oldest aged 40 years), and three recorded cases have affected African elephants. [4] [6] The first documented fatal case for African elephants was Kijana, an eleven-month-old male in 1996. [4] [11] Since 2008, a number of cases have been attributed to EEHV1 among wild Asian elephants. [4] [23]

The first suspected case in Asia was in 1997, though it was not until the fifth suspected case that the presence of the virus could be confirmed. This case was reported in 2006, with the death of a young wild-born female calf at an elephant sanctuary in Cambodia. The virus was identified as part of the EEHV1 group, the same as previously identified in the North American and European captive populations. [24] In 2013, nine lethal cases from India were extensively characterized and found to consist of a wide variety of genetically diverged strains of EEHV1A and EEHV1B matching the subtypes and genetic range of nearly all those found previously in Europe and North America. [25] Cases attributed to EEHV1A and EEHV4 have also been reported in Thailand [26] and there is both confirmed and anecdotal evidence for similar hemorrhagic disease deaths of between 16 and 30 more calves in Asian countries including Thailand, India, Nepal, Myanmar and Indonesia within the past five years. Thus, this is not just a disease of captive elephants, but is endogenous to and possibly rampant in Asian elephants in the wild also. [27] Further research has been noted as "urgently required" to study the situation in regions with wild Asian elephant populations. [4]

On 12 June 2019 it was reported [28] that in Chester Zoo the 2-year-old Indian elephant calf Indali Hi Way had fully recovered from EEHV, after numerous treatments over 2 weeks, and that there is now hope of a vaccine for EEHV.

In 2020, a 1-year-old Asian elephant named Ajay, from the Rosamond Gifford Zoo in Syracuse, New York, which was popular in the area, died from the virus. [29] [30]

In July 2024 Dublin Zoo reported two deaths from the virus. [31] Avani who was 8 years old and Zinda who was 7 both passed away from the virus.

Related Research Articles

<span class="mw-page-title-main">Asian elephant</span> Second largest elephant species

The Asian elephant, also known as the Asiatic elephant, is a species of elephant distributed throughout the Indian subcontinent and Southeast Asia, from India in the west to Borneo in the east, and Nepal in the north to Sumatra in the south. Three subspecies are recognised—E. m. maximus, E. m. indicus and E. m. sumatranus. The Asian elephant is characterised by its long trunk with a single finger-like processing; large tusks in males; laterally folded large ears but smaller in contrast to African elephants; and wrinkled grey skin. The skin is smoother than African elephants and may be depigmented on the trunk, ears or neck. Adult males average 4 t in weight, and females 2.7 t.

<i>Herpesviridae</i> Family of DNA viruses

Herpesviridae is a large family of DNA viruses that cause infections and certain diseases in animals, including humans. The members of this family are also known as herpesviruses. The family name is derived from the Greek word ἕρπειν, referring to spreading cutaneous lesions, usually involving blisters, seen in flares of herpes simplex 1, herpes simplex 2 and herpes zoster (shingles). In 1971, the International Committee on the Taxonomy of Viruses (ICTV) established Herpesvirus as a genus with 23 viruses among four groups. As of 2020, 115 species are recognized, all but one of which are in one of the three subfamilies. Herpesviruses can cause both latent and lytic infections.

Bovine alphaherpesvirus 1 (BoHV-1) is a virus of the family Herpesviridae and the subfamily Alphaherpesvirinae, known to cause several diseases worldwide in cattle, including rhinotracheitis, vaginitis, balanoposthitis, abortion, conjunctivitis, and enteritis. BoHV-1 is also a contributing factor in shipping fever, also known as bovine respiratory disease (BRD). It is spread horizontally through sexual contact, artificial insemination, and aerosol transmission and it may also be transmitted vertically across the placenta. BoHV-1 can cause both clinical and subclinical infections, depending on the virulence of the strain. Although these symptoms are mainly non-life-threatening it is an economically important disease as infection may cause a drop in production and affect trade restrictions. Like other herpesviruses, BoHV-1 causes a lifelong latent infection and sporadic shedding of the virus. The sciatic nerve and trigeminal nerve are the sites of latency. A reactivated latent carrier is normally the source of infection in a herd. The clinical signs displayed are dependent on the virulence of the strain. There is a vaccine available which reduces the severity and incidence of disease. Some countries in Europe have successfully eradicated the disease by applying a strict culling policy.

Aujeszky's disease, usually called pseudorabies in the United States, is a viral disease in swine that is endemic in most parts of the world. It is caused by Suid herpesvirus 1 (SuHV-1). Aujeszky's disease is considered to be the most economically important viral disease of swine in areas where classical swine fever has been eradicated. Other mammals, such as cattle, sheep, goats, cats, dogs, and raccoons, are also susceptible. The disease is usually fatal in these animal species.

<span class="mw-page-title-main">Feline viral rhinotracheitis</span> Infectious disease of cats

Feline viral rhinotracheitis (FVR) is an upper respiratory or pulmonary infection of cats caused by Felid alphaherpesvirus 1 (FeHV-1), of the family Herpesviridae. It is also commonly referred to as feline influenza, feline coryza, and feline pneumonia but, as these terms describe other very distinct collections of respiratory symptoms, they are misnomers for the condition. Viral respiratory diseases in cats can be serious, especially in catteries and kennels. Causing one-half of the respiratory diseases in cats, FVR is the most important of these diseases and is found worldwide. The other important cause of feline respiratory disease is feline calicivirus.

<span class="mw-page-title-main">Bovine malignant catarrhal fever</span> Species of virus

Bovine malignant catarrhal fever (BMCF) is a fatal lymphoproliferative disease caused by a group of ruminant gamma herpes viruses including Alcelaphine gammaherpesvirus 1 (AlHV-1) and Ovine gammaherpesvirus 2 (OvHV-2) These viruses cause unapparent infection in their reservoir hosts, but are usually fatal in cattle and other ungulates such as deer, antelope, and buffalo. In Southern Africa the disease is known as snotsiekte, from the Afrikaans.

<i>Gammaherpesvirinae</i> Subfamily of viruses

Gammaherpesvirinae is a subfamily of viruses in the order Herpesvirales and in the family Herpesviridae. Viruses in Gammaherpesvirinae are distinguished by reproducing at a more variable rate than other subfamilies of Herpesviridae. Mammals serve as natural hosts. There are 43 species in this subfamily, divided among 7 genera with three species unassigned to a genus. Diseases associated with this subfamily include: HHV-4: infectious mononucleosis. HHV-8: Kaposi's sarcoma.

Bovine alphaherpesvirus 5 (BoHV-5) is a virus species of the genus Varicellovirus and subfamily Alphaherpesvirinae. It causes meningoencephalitis and respiratory disease in cattle and sheep. As with all herpes viruses latent infection can occur, with recrudescence at times of stressed and/or immunosuppression. Sites of latency include the CNS and mucosae of the nose and trachea. The disease has been documented in South America, the United States, Australia, Germany and Hungary. Caused by: BHV-5 – Bovine Encephalitis Virus – Bovine Encephalitis Herpesvirus

<span class="mw-page-title-main">B virus</span> Species of virus

B-virus, Herpesvirus simiae, or Herpes virus B is the Simplexvirus infecting macaque monkeys. B virus is very similar to HSV-1, and as such, this neurotropic virus is not found in the blood.

<i>Alcelaphine gammaherpesvirus 2</i> Species of virus

Alcelaphine gammaherpesvirus 2 (AlHV-2) is a species of Macavirus that is believed to be responsible for causing hartebeest infections of malignant catarrhal fever.

Human betaherpesvirus 7 (HHV-7) is one of nine known members of the Herpesviridae family that infects humans. HHV-7 is a member of Betaherpesvirinae, a subfamily of the Herpesviridae that also includes HHV-6 and Cytomegalovirus. HHV-7 often acts together with HHV-6, and the viruses together are sometimes referred to by their genus, Roseolovirus. HHV-7 was first isolated in 1990 from CD4+ T cells taken from peripheral blood lymphocytes.

Haemorrhagic septicaemia (HS) is one of the most economically important pasteurelloses. Haemorrhagic septicaemia in cattle and buffaloes was previously known to be associated with one of two serotypes of P. multocida: Asian B:2 and African E:2 according to the Carter-Heddleston system, or 6:B and 6:E using the Namioka-Carter system.

Malacoherpesviridae is a family of DNA viruses in the order Herpesvirales. Molluscs serve as natural hosts, making members of this family the only known herpesviruses to infect invertebrates. There are currently only two species recognised in this family, both classified into separate genera. Disease associated with this family includes sporadic episodes of high mortality among larvae and juveniles. The family name Malacoherpesviridae is derived from Greek word 'μαλακός (malacos) meaning 'soft' and from Greek word 'μαλάκιον (malakion) meaning 'mollusc'.

<span class="mw-page-title-main">International Elephant Foundation</span>

The International Elephant Foundation (IEF) is a non-profit 501(c)(3) corporation. Formed by individuals and institutions, IEF is dedicated to the conservation of African and Asian elephants worldwide.

Pacheco's disease is a highly infectious and acute bird disease caused by a species of herpesvirus, Psittacid alphaherpesvirus 1 (PsHV-1). All psittacine species are susceptible to Pacheco's disease, mainly those in zoological collections and aviaries in any geographic regions. Pacheco's disease most commonly occurs in Amazon parrots, followed by African grey parrots, parrots, macaws, cockatoos and conures. Due to a very high mortality rate within these susceptible species, concerns are brought to companion bird markets and breeders.

<span class="mw-page-title-main">Captive elephants</span> Elephants kept in a confined area

Elephants can be found in various captive facilities such as a zoo, sanctuary, circus, or camp, usually under veterinary supervision. They can be used for educational, entertainment, or work purposes.

Proboscivirus is a genus of viruses in the order Herpesvirales, in the family Herpesviridae, in the subfamily Betaherpesvirinae. Elephants serve as natural hosts. EEHV1 is apathogenic for African elephants but causes fatal haemorrhagic disease in Asian elephants. The name "Proboscivirus" comes from the Greek word προβοσκίς or "proboscis" meaning "the elephant trunk," for which the virus accordingly uses as its means of contraction and transmission to enter the elephant's body.

Batravirus ranidallo1, also known as Ranid herpesvirus 1 (RaHV-1), is a double-stranded DNA virus within the order Herpesvirales. The virus was initially observed within renal tumors in 1934 by Baldwin Lucké, and more recently has become identifiable through the use of PCR in samples isolated from frog tumors. RaHV-1 causes renal tumors within the northern leopard frog, Rana pipiens. The virus has not yet been isolated in vitro within cell lines, meaning that while its existence and symptoms are fairly evident, its methods of transmission, cell infection, and reproduction are largely unknown.

Caprine alphaherpesvirus 1 (CpHV-1) is a species of virus known to infect goats worldwide. It has been shown to produce systemic and respiratory symptoms in kids and to cause abortions in adult goats.

Thomas B. Hildebrandt is a German veterinarian researcher dedicated to species conservation. He heads the Department of Reproduction Management at the Leibniz Institute for Zoo and Wildlife Research (IZW) in Berlin and holds a full professorship for Wildlife Reproduction Medicine at the veterinary faculty of the Freie Universität Berlin.

References

  1. Davison, Andrew (27 January 2016). "Rename species in the family Herpesviridae to incorporate a subfamily designation" (PDF). International Committee on Taxonomy of Viruses (ICTV). p. 3. Retrieved 10 July 2019. BetaherpesvirinaeProboscivirusElephantid herpesvirus 1Elephantid betaherpesvirus 1
  2. Ossent, P.; Guscetti, F.; Metzler, A. E.; Lang, E. M.; Rübel, A.; Hauser, B. (March 1990). "Acute and Fatal Herpesvirus Infection in a Young Asian Elephant (Elephas maximus)". Veterinary Pathology. 27 (2): 131–133. doi:10.1177/030098589002700212. ISSN   0300-9858. PMID   2161138. S2CID   37224170.
  3. Database entry at elephant.se
  4. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 Koehl, Dan (2009). "EEHV - Elephant endotheliotropic herpes virus". elephant.se. Retrieved 2009-05-07.
  5. 1 2 3 Latimer E; Zong JC; Heaggans SY; Richman LK; Hayward GS (2011). "Detection and evaluation of novel herpesviruses in routine and pathological samples from Asian and African elephants: Identification of two new probosciviruses (EEHV5 and EEHV6) and two new gammaherpesviruses (EGHV3B and EGHV5)". Veterinary Microbiology. 147 (1–2): 28–41. doi:10.1016/j.vetmic.2010.05.042. PMC   2976818 . PMID   20579821.
  6. 1 2 3 Zong J-C; Latimer E; Heaggans SY; Richman LK; Hayward GS (2007). Pathogenesis and Molecular Epidemiology of Fatal Elephant Endotheliotrophic Disease Associated with the Expanding Proboscivirus Genus of the Betaherpesvirinae. Proc. Internat. Elephant Conservation and Res. Symp, Orlando, Florida. pp. 23–35.
  7. 1 2 3 Fickel J, Richman LK, Montali R, Schaftenaar W, Göritz F, Hildebrandt TB, Pitra C (2001). "A variant of the endotheliotropic herpesvirus in Asian elephants (Elephas maximus) in European zoos". Veterinary Microbiology. 82 (2): 103–109. doi:10.1016/S0378-1135(01)00363-7. PMID   11423201.
  8. 1 2 3 4 5 6 7 8 Mikota, Susan (2007). "Endotheliotropic Herpesvirus (EEHV)". Elephant Care International Fact Sheets. Elephant Care International. Archived from the original on 2006-02-23. Retrieved 2009-05-07.
  9. 1 2 Cracknell, Jonathan (2008). "Herpes-viruses in Asian elephants (abstract)" (PDF). Archived from the original (PDF) on 2016-03-03. Retrieved 2009-05-11.
  10. Zong, J-C; Latimer E; Heaggans SY; Richman LK & Hayward GS (2008). Viral Gene Subtyping of Eighteen North American Cases of EEHV Hemorrhagic Disease. International Elephant Conservation and Research Symposium, Bangkok, Thailand.
  11. 1 2 3 Richman LK; Montali RJ; Garber RL; Kennedy MA; Lehnhardt J; Hildebrandt T; Schmitt D; Hardy D; Alcendor DJ; Hayward GS (1999). "Novel endotheliotropic herpesviruses fatal for Asian and African elephants". Science. 283 (5405): 1171–1176. Bibcode:1999Sci...283.1171R. doi:10.1126/science.283.5405.1171. PMID   10024244.
  12. Richman LK; Montali RJ; Cambre RC; Schmitt D; Hardy D; Hildbrandt T; Bengis RG; Hamzeh FM; Shahkolahi A; Hayward GS (2000). "Clinical and pathological findings of a newly recognized disease of elephants caused by endotheliotropic herpesviruses". Journal of Wildlife Diseases. 36 (1): 1–12. doi: 10.7589/0090-3558-36.1.1 . PMID   10682740.
  13. Ehlers B.; Dural G.; Marschall M. (2006). "Endotheliotropic elephant herpesvirus, the first betaherpesvirus with a thymidine kinase gene". Journal of General Virology. 87 (Pt 10): 2781–2789. doi: 10.1099/vir.0.81977-0 . PMID   16963736.
  14. Garner MM, Helmick K, Ochsenrieter J, Richman LK, Latimer E, Wise AG, Maes K, Kuipel M, Nordhausen RW, Zong J-C, Hayward GS (2009). "Clinico-pathologic Features of Fatal Disease Attributed to New Variants of Endotheliotropic Herpesviruses in Two Asian Elephants (Elephas maximus)". Veterinary Pathology. 46 (1): 97–104. doi:10.1354/vp.46-1-97. PMC   3572918 . PMID   19112123.
  15. Denk D; Stidworthy MF; Redrobe E; Latimer E; Hayward GS; Cracknell J; Classens A; Steinbach F; McGowan S; Dasterjerdi A (2012). "Fatal elephant endotheliotropic herpesvirus type 5 infection in a captive Asian elephant". The Veterinary Record. 148 (15): 380–381. doi:10.1136/vr.e6833. PMID   23065589. S2CID   30781584.
  16. Zong et al, 2010
  17. Wellehan JFX; Johnson AJ; Childressa AL; Harr KE; Isaza R (2008). "Six novel gammaherpesviruses of Afrotheria provide insight into the early divergence of the Gammaherpesvirinae". Veterinary Microbiology. 127 (3–4): 249–257. doi:10.1016/j.vetmic.2007.08.024. PMID   17884307.
  18. Stanton JJ, Zong JC, Latimer E, Tan J, Herron A, Hayward GS, Ling PD (2010). "Detection of pathogenic elephant endotheliotropic herpesvirus in routine trunk washes from healthy adult Asian elephants (Elephas maximus) by use of a real-time quantitative polymerase chain reaction assay". American Journal of Veterinary Research. 71 (8): 925–933. doi:10.2460/ajvr.71.8.925. PMC   3725808 . PMID   20673092.
  19. Stanton JJ; Zong J-C; Eng C; Howard L; Flanagan J; Stevens S; Schmitt D; Weidner E; Graham D; Junge R; Weber ME; Fischer M; Meija A; Tan J; Latimer E; Herron A; Hayward GS; Ling PD (2013). "Kinetics of viral loads and genotypic analysis of elephant endotheliotropic herpesvirus-1 infection in captiveAsian elephants (Elephas maximus)". Journal of Zoo and Wildlife Medicine. 44 (1): 42–54. doi:10.1638/1042-7260-44.1.42. PMC   3746492 . PMID   23505702.
  20. Atkins L; Zong J-C; Tan J; Meija A; Heaggans SY; Nofs S; Stanton JJ; Flanagan JP; Howard L; Latimer E; Stevens MR; Hoffman DS; Hayward GS; Ling PD (2013). "EEHV-5, A newly recognized elephant herpesvirus associated with clinical and sub-clinical infections in captive Asian elephants (Elephas maximus)". Journal of Zoo and Wildlife Medicine. 44 (1): 136–143. doi:10.1638/1042-7260-44.1.136. PMC   3746547 . PMID   23505714.
  21. 1 2 3 "Tracking an Elephant Killer". Spotlight on Zoo Science. National Zoological Park. 2005-04-01. Archived from the original on 2009-05-02. Retrieved 2009-05-10.
  22. Akst, Jef (2015-06-01). "A Plague on Pachyderms". the-scientist.com.
  23. Zachariah A; Richman LK; Latimer E; Hayward GS; Kalaivannan N; Zachariah A; Balan S (2008). Fatal Endotheliotropic Elephant Herpes Virus Infection in Captive and Free-ranging Asian Elephants in South India. International Elephant Conservation and Research Symposium, Bangkok, Thailand.
  24. Reid CE, Hildebrandt TB, Marx N, Hunt M, Thy N, Reynes JM, Schaftenaar W, Fickel J (2006). "Endotheliotropic elephant herpes virus (EEHV) infection. The first PCR-confirmed fatal case in Asia". Veterinary Quarterly. 28 (2): 61–64. doi:10.1080/01652176.2006.9695209. PMID   16841568. S2CID   25537428.
  25. Zachariah A; Zong J-C; Long SY; Latimer EM; Heaggans SY; Richman LK; Hayward GS (2013). "Fatal herpesvirus (EEHV) hemorrhagic disease in wild and orphan Asian elephants in southern India". Journal of Wildlife Diseases. 49 (2): 381–393. doi:10.7589/2012-07-193. PMC   3707512 . PMID   23568914.
  26. Sripiboon S; Tanjaew P; Lungka G; Thitaram C (2013). "(Case Report) The occurrence of elephant herpesviruses in captive Asian elephants: the first case of EEHV4 in Asia". Journal of Zoo and Wildlife Medicine. 44 (1): 100–104. doi:10.1638/1042-7260-44.1.100. PMID   23505709. S2CID   44649231.
  27. Hayward GS (2012). "Conservation:clarifying the risk from herpesvirus to captive Asian elephants". The Veterinary Record. 212 (8): 202–203. doi:10.1136/vr.e1212. PMC   3587150 . PMID   22368209.
  28. "Elephant's virus survival 'momentous'". BBC News. 2019-06-12.
  29. "Rosamond Gifford Zoo Mourns Loss of Elephant Calf to Herpes Virus". Rosamond Gifford Zoo. Retrieved 2024-02-28.
  30. CNYCentral (2020-12-09). "Baby elephant Ajay dies at Rosamond Gifford Zoo in Syracuse". WSTM. Retrieved 2024-02-28.
  31. "Dublin Zoo announces death of seven-year-old elephant". RTÉ News. 7 July 2024. Retrieved 8 July 2024.