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Journal of Zoo and Wildlife Medicine | 2013

KINETICS OF VIRAL LOADS AND GENOTYPIC ANALYSIS OF ELEPHANT ENDOTHELIOTROPIC HERPESVIRUS-1 INFECTION IN CAPTIVE ASIAN ELEPHANTS (ELEPHAS MAXIMUS)

Jeffrey J. Stanton; Jian Chao Zong; Crystal Eng; Lauren Howard; Joe Flanagan; Martina Stevens; Dennis L. Schmitt; Ellen Wiedner; Danielle Graham; Randall E. Junge; Martha Weber; Martha T. Fischer; Alicia Mejia; Jie Tan; Erin Latimer; Alan Herron; Gary S. Hayward; Paul D. Ling

Abstract:  Elephant endotheliotropic herpesviruses (EEHVs) can cause fatal hemorrhagic disease in juvenile Asian elephants (Elephas maximus); however, sporadic shedding of virus in trunk washes collected from healthy elephants also has been detected. Data regarding the relationship of viral loads in blood compared with trunk washes are lacking, and questions about whether elephants can undergo multiple infections with EEHVs have not been addressed previously. Real-time quantitative polymerase chain reaction was used to determine the kinetics of EEHV1 loads, and genotypic analysis was performed on EEHV1 DNA detected in various fluid samples obtained from five Asian elephants that survived detectable EEHV1 DNAemia on at least two separate occasions. In three elephants displaying clinical signs of illness, preclinical EEHV1 DNAemia was detectable, and peak whole-blood viral loads occurred 3–8 days after the onset of clinical signs. In two elephants with EEHV1 DNAemia that persisted for 7–21 days, no clinical signs of illness were observed. Detection of EEHV1 DNA in trunk washes peaked approximately 21 days after DNAemia, and viral genotypes detected during DNAemia matched those detected in subsequent trunk washes from the same elephant. In each of the five elephants, two distinct EEHV1 genotypes were identified in whole blood and trunk washes at different time points. In each case, these genotypes represented both an EEHV1A and an EEHV1B subtype. These data suggest that knowledge of viral loads could be useful for the management of elephants before or during clinical illness. Furthermore, sequential infection with both EEHV1 subtypes occurs in Asian elephants, suggesting that they do not elicit cross-protective sterilizing immunity. These data will be useful to individuals involved in the husbandry and clinical care of Asian elephants.


Journal of Zoo and Wildlife Medicine | 2013

ELEPHANT ENDOTHELIOTROPIC HERPESVIRUS 5, A NEWLY RECOGNIZED ELEPHANT HERPESVIRUS ASSOCIATED WITH CLINICAL AND SUBCLINICAL INFECTIONS IN CAPTIVE ASIAN ELEPHANTS (ELEPHAS MAXIMUS)

Lisa M. Atkins; Jian Chao Zong; Jie Tan; Alicia Mejia; Sarah Y. Heaggans; Sally A. Nofs; Jeffrey J. Stanton; Joseph P. Flanagan; Lauren Howard; Erin Latimer; Martina Stevens; Daryl S. Hoffman; Gary S. Hayward; Paul D. Ling

Abstract:  Elephant endotheliotropic herpesviruses (EEHVs) can cause acute hemorrhagic disease with high mortality rates in Asian elephants (Elephas maximus). Recently, a new EEHV type known as EEHV5 has been described, but its prevalence and clinical significance remain unknown. In this report, an outbreak of EEHV5 infection in a herd of captive Asian elephants in a zoo was characterized. In February 2011, a 42-yr-old wild-born female Asian elephant presented with bilaterally swollen temporal glands, oral mucosal hyperemia, vesicles on the tongue, and generalized lethargy. The elephant had a leukopenia and thrombocytopenia. She was treated with flunixin meglumine, famciclovir, and fluids. Clinical signs of illness resolved gradually over 2 wk, and the white blood cell count and platelets rebounded to higher-than-normal values. EEHV5 viremia was detectable starting 1 wk before presentation and peaked at the onset of clinical illness. EEHV5 shedding in trunk secretions peaked after viremia resolved and continued for more than 2 mo. EEHV5 trunk shedding from a female herd mate without any detectable viremia was detected prior to onset of clinical disease in the 42-yr-old elephant, indicating reactivation rather than primary infection in this elephant. Subsequent EEHV5 viremia and trunk shedding was documented in the other five elephants in the herd, who remained asymptomatic, except for 1 day of temporal gland swelling in an otherwise-healthy 1-yr-old calf. Unexpectedly, the two elephants most recently introduced into the herd 40 mo previously shed a distinctive EEHV5 strain from that seen in the other five elephants. This is the first report to document the kinetics of EEHV5 infection in captive Asian elephants and to provide evidence that this virus can cause illness in some animals.


Journal of Zoo and Wildlife Medicine | 2004

SERUM CONCENTRATIONS OF IONIZED CALCIUM, VITAMIN D3, AND PARATHYROID HORMONE IN CAPTIVE THICK-BILLED PARROTS (RHYNCHOPSITTA PACHYRHYNCHA)

Lauren Howard; Philip H. Kass; Nadine Lamberski; Ray F. Wack

Abstract Serum collected from 68 thick-billed parrots (Rhynchopsitta pachyrhyncha) from 15 institutions was analyzed for ionized Ca (iCa), total Ca (tCa), P, total protein (TP), albumin (Alb), parathyroid hormone (PTH), and vitamin D3. Values were not distributed normally; 95% frequency intervals were as follows: iCa (0.82–1.3 mmol/L), tCa (1.37–2.09 mmol/L,), P (0.35–1.75 mmol/L), TP (21–39 g/L), Alb (9–13 g/L), PTH (0–65.68 pmol/L), and vitamin D3 (5.2–51 nmol/L). Sixty percent (±7.5%) of tCa was ionized. Female thick-billed parrots had significantly higher mean iCa (1.11 mmol/L, n = 22) than male thick-billed parrots (1.05 mmol/L, n = 32). tCa and iCa values in thick-billed parrots were lower than the reported values for other psittacine species. A significant positive linear relationship existed between Alb–TP and iCa–tCa ratios. A significant inverse linear relationship was also identified between the tCa–P ratio and PTH. These findings are consistent with known domestic avian Ca physiology.


Journal of Zoo and Wildlife Medicine | 2008

Yolk Coelomitis in Fiji Island Banded Iguanas (Brachylophus fasciatus)

Brian A. Stacy; Lauren Howard; John Kinkaid; Justin D. Vidal; Rebecca Papendick

Abstract Yolk coelomitis is a major cause of death in captive sexually mature female Fiji Island banded iguanas (Brachylophus fasciatus) maintained by the Zoological Society of San Diego. The medical records, breeding histories, and pathology archival materials from this group were reviewed to study this health problem. From 1987 through 2004, deaths of nine of 21 adult females were due to yolk coelomitis. Most iguanas had a history of reproduction-related problems, which included reproductive failure, episodes of lethargy associated with ovarian activity, folliculostasis, ovostasis, and behavioral abnormalities. Most affected iguanas either were found dead or presented moribund and subsequently died or were euthanized. Clinical signs were nonspecific and included lethargy, cutaneous discoloration, and coelomic effusion. Yolk leakage in most cases was associated with the presence of large vitellogenic follicles undergoing atresia and resulted in coelomitis characterized by florid mesothelial proliferation.


Journal of Zoo and Wildlife Medicine | 2004

Chemical immobilization of rhebok (Pelea capreolus) with carfentanil-xylazine or etorphine-xylazine.

Lauren Howard; Karen S. Kearns; Tracy L. Clippinger; R. Scott Larsen; Patrick J. Morris

Abstract Twelve adult rhebok (Pelea capreolus) were immobilized using a combination of 0.4 mg/kg xylazine and either 0.01 mg/kg of carfentanil (n = 6) or 0.01 mg/kg etorphine (n = 6), delivered i.m. using a remote injection system. Induction and recovery times, heart rate, respiratory rate, rectal temperature, oxygen saturation, end-tidal CO2 (ETCO2), anesthetic depth, indirect blood pressure, and arterial blood gases were recorded. Rhebok were not intubated but nasal oxygen was administered. Forty minutes after induction, anesthesia was antagonized with naltrexone and yohimbine. Mean initial heart rate was significantly higher in the carfentanil group than in the etorphine group. Mean initial oxygen saturation was consistent with hypoxia in both the carfentanil group and the etorphine group. In both groups, arterial pH decreased and partial pressure of carbon dioxide increased during the first 15 min of anesthesia, and values were similar in both groups. These findings were consistent with respiratory acidosis and decreased ventilation. Values for respiratory rate, temperature, oxygen saturation, ETCO2, and blood pressure were similar for both groups at all time periods. During the first 5 min of anesthesia, rhebok in the carfentanil group were more responsive to stimuli than rhebok in the etorphine group. After administration of antagonists, time to first arousal was significantly shorter in the etorphine group than in the carfentanil group. Although cardiopulmonary values were similar for the two groups, rhebok in the carfentanil group were at a comparatively lighter plane of anesthesia, and some individuals in this group required additional manual and chemical restraint for medical procedures to be performed. In conclusion, for captive adult rhebok, 0.01 mg/kg of etorphine and 0.4 mg/kg of xylazine are recommended over 0.01 mg/kg carfentanil and 0.4 mg/kg xylazine because of qualitatively better anesthetic episodes and shorter recovery times.


Journal of Zoo and Wildlife Medicine | 2016

CLINICAL INFECTION OF CAPTIVE ASIAN ELEPHANTS (ELEPHAS MAXIMUS) WITH ELEPHANT ENDOTHELIOTROPIC HERPESVIRUS 4

Angela Fuery; Geoffrey R. Browning; Jie Tan; Simon Y. Long; Gary S. Hayward; Sherry K. Cox; Joseph P. Flanagan; Maryanne E. Tocidlowski; Lauren Howard; Paul D. Ling

Abstract Elephant endotheliotropic herpesvirus (EEHV) can cause lethal hemorrhagic disease in juvenile Asian elephants. A number of EEHV types and subtypes exist, where most deaths have been caused by EEHV1A and EEHV1B. EEHV4 has been attributed to two deaths, but as both diagnoses were made postmortem, EEHV4 disease has not yet been observed and recorded clinically. In this brief communication, two cases of EEHV4 infection in juvenile elephants at the Houston Zoo are described, where both cases were resolved following intensive treatment and administration of famciclovir. A quantitative real-time polymerase chain reaction detected EEHV4 viremia that correlated with clinical signs. High levels of EEHV4 shedding from trunk wash secretions of the first viremic elephant correlated with subsequent infection of the second elephant with EEHV4. It is hoped that the observations made in these cases—and the successful treatment regimen used—will help other institutions identify and treat EEHV4 infection in the future.


Veterinary Immunology and Immunopathology | 2013

Prenatal passive transfer of maternal immunity in Asian elephants (Elephas maximus)

Sally A. Nofs; Robert L. Atmar; Wendy A. Keitel; Cathleen A. Hanlon; Jeffrey J. Stanton; Jie Tan; Joseph P. Flanagan; Lauren Howard; Paul D. Ling

Asian (Elephas maximus) and African (Loxodonta africana) elephants exhibit characteristics of endotheliochorial placentation, which is common in carnivore species and is associated with modest maternal to fetal transplacental antibody transfer. However, it remains unknown whether the bulk of passive immune transfer in elephants is achieved prenatally or postnatally through ingestion of colostrum, as has been documented for horses, a species whose medical knowledgebase is often extrapolated for elephants. To address this issue, we took advantage of the fact that many zoo elephants are immunized with tetanus toxoid and/or rabies vaccines as part of their routine health care, allowing a comparison of serum antibody levels against these antigens between dams and neonates. Serum samples were collected from 3 newborn Asian elephant calves at birth (before ingestion of colostrum); 2-4 days after birth; and 2-3 months of age. The findings indicate that the newborns had anti-tetanus toxoid and anti-rabies titers that were equivalent to or higher than the titers of their dams from birth to approximately 3 months of age, suggesting that the majority of maternal-to-fetal transfer is transplacental and higher than expected based on the architecture of the Asian elephant placenta.


Journal of Zoo and Wildlife Medicine | 2005

SERUM GAMMA-GLUTAMYLTRANSFERASE AS A PROGNOSTIC INDICATOR OF NEONATAL VIABILITY IN NONDOMESTIC RUMINANTS

Lauren Howard; Leslie M. Turner; Ilse H. Stalis; Patrick J. Morris

Abstract Rapid assessment of immune status in neonatal ruminants of endangered species facilitates early intervention in cases of inadequate passive transfer of maternal immunoglobulins. Serum gamma-glutamyltransferase (GGT) was used to evaluate suspected passive transfer status in 25 North Indian muntjac (Muntiacus muntjak vaginalis), 45 Cretan goats (Capra algagrus cretica), 20 white-lipped deer (Cervus albirostris), 25 Mhorr gazelles (Gazella dama mhorr), and 31 Soemmerrings gazelles (Gazella soemmerringi soemmerringi). Serum GGT, measured within 48 hr of birth, was compared with clinical condition at 5 days of age. Neonatal Soemmerrings and Mhorr gazelles with GGT >600 U/L were likely to survive without medical intervention, whereas GGT <400 U/L was a good indicator that the gazelle neonate would need medical intervention. Neonatal muntjac with GGT >200 U/L were also likely to survive without medical intervention. Because there is no gold standard for evaluating passive transfer status in neonatal nondomestic ruminants, it is recommended to evaluate the results of more than one diagnostic test, as well as clinical condition, in considering health status and disposition of neonatal ruminants of endangered species.


Journal of Zoo and Wildlife Medicine | 2005

TRANSPOSITION OF THE BICEPS TENDON TO REDUCE LATERAL SCAPULOHUMERAL LUXATION IN THREE SPECIES OF NONDOMESTIC RUMINANT

Lauren Howard; G. Lynn Richardson

Abstract Open reduction of lateral luxation of the scapulohumeral joint was performed in a Mhorr gazelle (Gazella dama mhorr), a southern pudu (Pudu puda), and an Alpine ibex (Capra ibex ibex) by transposition of the biceps brachii tendon lateral to the greater tubercle of the humerus. The ibex had a very large greater tubercle that required a second osteotomy to allow successful lateral transfer of the tendon. Although all three animals were non–weight bearing in the first 2–3 wk after surgery, ambulation improved at 3 wk and was almost normal by 6 wk after surgery. Postoperative follow-up of 8 yr, 7 mo, and 3 mo in the gazelle, pudu, and ibex, respectively, revealed normal ambulation with no gait deficits. The gazelle was euthanized 8 yr after surgery for unrelated disease and necropsy demonstrated mild to moderate degenerative joint disease. Similar lateral shoulder luxations in comparably sized, nondomestic ruminants, without concurrent fractures or significant joint abnormality, have a good prognosis for return to function after surgical reduction using a biceps tendon transposition.


Journal of Zoo and Wildlife Medicine | 2016

THE IMPACT OF ELEPHANT ENDOTHELIOTROPIC HERPESVIRUS ON THE CAPTIVE ASIAN ELEPHANT (ELEPHAS MAXIMUS) POPULATION OF THE UNITED KINGDOM AND IRELAND (1995–2013)

Rebecca Kendall; Lauren Howard; Nic Masters; Robyn A. Grant

Abstract Elephant endotheliotropic herpesvirus (EEHV) is one of the most devastating infections and causes of mortality in captive Asian elephant (Elephas maximus) populations. Eight confirmed fatal EEHV cases have occurred since 1995 within the captive Asian elephant population of the United Kingdom and Ireland. This report aims to review the impact of EEHV on the captive Asian elephant population in the United Kingdom and Ireland, document and compare fatal cases, and recommend a framework of monitoring within the United Kingdom and Ireland to increase the success of treatment of EEHV hemorrhagic disease (EEHV HD) in the future. Six zoologic institutions (which include zoos, safari parks, and wildlife parks) that currently house or have previously housed a captive Asian elephant group were included in this report. Medical records and postmortem results were collected from four of these institutions for each confirmed fatal case. EEHV HD was found to be responsible for 29.6% of fatalities in Asian elephants born in captivity in the United Kingdom and Ireland between 1995 and 2013. Following a review of all the cases, it is shown that although clinical signs may be associated with specific EEHV species, the swiftness of disease progression means that most body tissues are impacted 1–6 days following the presentation of visible clinical signs and treatment is less likely to succeed. Therefore, EEHV monitoring should consist of conducting regular polymerase chain reaction analysis of whole blood samples from at-risk, young Asian elephants aged 1–8 yr in order for subclinical viremia to be identified early and treatment to be started before the appearance of visible clinical signs.

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Erin Latimer

Smithsonian Conservation Biology Institute

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Jie Tan

Baylor College of Medicine

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Nic Masters

Zoological Society of London

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Alicia Mejia

Baylor College of Medicine

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Sally A. Nofs

Baylor College of Medicine

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