FATAL ENCEPHALOMYOCARDITIS VIRUS INFECTION IN AN AFRICAN SAVANNA ELEPHANT (LOXODONTA AFRICANA) IN A FRENCH ZOO Author(s): Benjamin Lamglait, D.V.M., M.Sc., Antoine Joris, D.V.M., Aurore Romey, Labib Bakkali-Kassimi, Ph.D., and Karin Lemberger, D.V.M., Dipl. A.C.V.P. Source: Journal of Zoo and Wildlife Medicine, 46(2):393-396. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/2014-0132R1.1 URL: http://www.bioone.org/doi/full/10.1638/2014-0132R1.1
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Zoo and Wildlife Medicine 46(2): 393–396, 2015 Copyright 2015 by American Association of Zoo Veterinarians
FATAL ENCEPHALOMYOCARDITIS VIRUS INFECTION IN AN AFRICAN SAVANNA ELEPHANT (LOXODONTA AFRICANA) IN A FRENCH ZOO Benjamin Lamglait, D.V.M., M.Sc., Antoine Joris, D.V.M., Aurore Romey, Labib Bakkali-Kassimi, Ph.D., and Karin Lemberger, D.V.M., Dipl. A.C.V.P.
Abstract: A fatal case of encephalomyocarditis virus (EMCV) involving an African elephant (Loxodonta africana) occurred in November 2013 at the Re´serve Africaine de Sigean, France. An adult female was found dead without any preliminary symptoms. Gross pathologic changes consisted of petechiae and hemorrhages on mucosae and internal organs, abundant transudate in the abdominal and pericardial cavities, and myocarditis. Histopathologic examination showed extensive degeneration and necrosis of ventricular cardiomyocytes with concurrent lymphoplasmocytic and eosinophilic infiltrate. An EMCV was isolated from several organs and considered the causative agent of the myocarditis. The same strain of virus was also isolated in rodents captured on zoo premises and considered to be the reservoir of the virus. To the authors’ knowledge, this is the first EMCV case in a captive African elephant in Europe. Key words: African elephant, death, encephalomyocarditis, Loxodonta africana, virus, zoo.
BRIEF COMMUNICATION The encephalomyocarditis virus (EMCV), genus Cardiovirus, family Picornaviridae, is a small nonenveloped, positive, single-stranded RNA virus that was first described in 1945. This virus is the causative agent of myocarditis and encephalitis but could also be responsible for reproductive disorders or diabetes in many mammalian species.1,3 The virus has an extremely broad host range, occurring in murid rodents, domestic and wild pigs, humans, and various captive species.1–3,5,8 Several outbreaks of fatal EMCV infections have been described in zoos in Australia, the United States, Italy, and Singapore.2,5,9–11 Sudden death was often the first indication of infection and was associated with acute fatal myocarditis. Although disease transmission is poorly understood, rodents are considered to be natural hosts of EMCV and thought to be the primary reservoir of the virus that might introduce and spread the virus by their infected carcasses or feces. These vectors contaminate feed and water, spreading the disease to susceptible animals.1,8
From the Re´serve Africaine de Sigean, 19 Chemin du hameau du lac, 11130 Sigean, France (Lamglait, Joris); UMR 1161 Virologie (Anses, Inra, Enva), ANSES–Laboratoire de Sante´ animale, 23 Avenue du Ge´ne´ral De Gaulle, 94700 Maisons-Alfort, France (Romey, Bakkali-Kassimi); and Vet Diagnostics, 14 Avenue Rockefeller, 69008 Lyon, France (Lemberger). Correspondence should be directed to Dr. Benjamin Lamglait ([email protected]).
This report describes the first EMCV infection in an African elephant (Loxodonta africana) housed in a French zoo. This case is described from a clinical, pathologic, and diagnostic point of view. Epidemiology and the role of rodents are also discussed. In November 2013, Seronga—an 18-yr-old wild-born female African elephant—was found dead without any preliminary symptoms. This individual had been transferred 1 mo before from a German zoo to the French institution at Sigean. She had adapted well to her new environment, though she appeared a bit more cautious than the other female that traveled with her. She was found dead in the morning, and the video recordings of the night revealed that she was active and ate with her cagemate until 6.00 AM, when she suddenly fell down. A full postmortem examination was performed. The main lesions consisted of petechiae and hemorrhages on the oral, ocular, rectal, and vaginal mucosae and on numerous internal organs such as spleen, heart, lymph nodes, large vessel walls, and mesovarium. There was also a marked cyanosis of her tongue, and a marked pulmonary congestion and edema. Abundant transudate was found in the abdominal cavity (about 100 L) and the pericardial cavity (about 20 L). Acute cardiac insufficiency was suspected. Some grey to white necrotic foci were seen in the myocardium, as well as petechiae and ecchymoses on the epicardial surface (Fig. 1). Because of the unspecific nature of the lesions observed, there are several differential diagnoses, including septicemia, viral infec-
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Figure 1. Petechiae and hemorrhages on oral mucosa and marked cyanosis of the tongue on an African elephant dead of EMCV infection. (Copyright B. Lamglait)
tion (elephant endotheliotrophic herpesvirus or encephalomyocarditis virus), or plant toxicity (mainly oleander). No clinical signs were noted on the other two African elephants held at the same institution. Bacteriology performed on several organs showed low quantities of nonspecific bacterial growth: Escherichia coli on the lungs and liver, considered contaminants; Pseudomonas aeruginosa on the trachea, also considered a contaminant because this bacteria is plant growth–promoting and no microscopic lesion was associated. The most significant lesions revealed by histopathology were extensive degeneration and necrosis of ventricular cardiomyocytes, with minimal infiltration by lymphocytes, macrophages, and fewer eosinophils and neutrophils (Fig. 2). Large areas of acute hemorrhages were noted in the adjacent epicardial adipose tissue and myocardium. Marked diffuse congestion and occasional hemorrhages and thrombosis were noted in other organs. The inflammatory microscopic lesions detected in the myocardium were consistent with an infectious etiology, particularly with a cardiovirus infection. For the virologic investigations, several tissues were tested by polymerase chain reaction (PCR) for elephant endotheliotropic herpesvirus (EEHV) 1–6, and all were negative. EMCV was detected by real-time reverse transcription (RT)PCR in the heart, kidney, and liver. The virus was
isolated on BHK-21 cells from the same organs and from blood and confirmed by sequencing. The death of this female African elephant occurred 1 mo after her arrival at Sigean. The transfer involved four females: two females were exchanged with two other females between Erfurt (Germany) and Sigean (France). Because the incubation period of EMCV is considered to be 9–45 days in rodents and pigs, a serological investigation was performed on all the females present in both institutions to determine where Seronga became infected. Only the two females from Sigean were positive for EMCV before the exchange. Another female who stayed at Erfurt had not seroconverted. Moreover, the EMCV serum neutralization test for Seronga was negative on the day of her death, demonstrating a recent infection. These findings suggest that the infection occurred at Sigean. Serum samples of elephants previously kept in Sigean were also tested to determine when the virus was present at the institution; it appears that EMCV has been present in Sigean since 2009. Because rodents are supposed to be the reservoir for EMCV, pest control was intensified. Additional traps were placed in the elephants’ premises to reduce the rodent population. Furthermore, food leftovers were systematically removed to avoid attracting rodents or contamination by their fomites. Mesenteric lymph node, sections of ileum, and feces from dead rats were collected for RT-PCR.
LAMGLAIT ET AL.—FATAL EMCV INFECTION IN AN AFRICAN ELEPHANT
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Figure 2. Histological findings on the myocardium of an African elephant dead of EMCV infection. H&E. (A) Necrosis of cardiomyocytes, 340 magnification. (B) Necrosis of cardiomyocytes with inflammation associated, 3400 magnification. (Courtesy of K. Lemberger)
EMCV was detected by real-time RT-PCR in feces of 6/21 (28.6%) rats, in mesenteric lymph nodes of 4/19 (21.1%) rats (Rattus norvegicus), and in ileum sections of 2/21 (2.5%) rats. Serum was also used to perform immunofluorescence assays for antibody detection. Of the 13 rats tested, 3 (23%) were positive and 2 more were equivocal. A literature review revealed numerous reports describing encephalomyocarditis virus (EMCV) as the etiological agent of viral myocarditis in free-ranging and captive exotic mammals. Primates seem to be affected worldwide and include lemurs (Eulemur spp., Lemur spp., and Varecia spp.), marmosets (Callithrix jacchus), squirrel monkeys (Saimiri boliviensis), macaques (Macaca sylvanus), baboons (Papio spp.), gibbons (Hylobates spp.), orangutans (Pongo pygmaeus), chimpanzees (Pan troglodytes), and bonobos (Pan paniscus).1,2,7,9,11 EMCV infection was also implicated in the death of various animals at Audubon Park Zoo, New Orleans, in 1985, including a Thomson’s gazelle (Eudorcas thompsonii) and a dromedary camel (Camelus dromedarius).1,11 Sporadic outbreaks of EMCV have occurred in Taronga Zoo, Australia, from 1987 to 1995, involving primates, a pigmy hippopotamus (Hexaprotodon liberiensis) and two Goodfellows tree-kangaroos (Dendrolagus goodfellowi).9 Fatal cases of encephalomyocarditis infections were described in four captive African elephants
held in two zoos in Florida in 1977;10 outbreaks of EMCV in the United States have been primarily restricted to the southeastern states, where they have been described in eight zoos in six states.4 An outbreak of EMCV occurred in Kruger National Park, South Africa, between 1993 and 1994 and was responsible for the deaths of 64 free-ranging adult African elephants.6 Most of them (83%) were adult bulls. As reported in our case, the most common clinical presentation was sudden death, or only mild unspecific clinical signs associated with congestive heart failure. Gross pathology described in several case reports consist of excessive pericardial fluid, epicardial hemorrhages, and pale foci within the myocardium. Microscopic changes include myofiber necrosis, edema, and mononuclear cell infiltration within the myocardium.2,9,11 Nevertheless, not all infections in elephants result in clinical disease, as shown by the prevalence of EMCV seropositivity in elephants in the Kruger National Park after the 1993–1994 EMCV outbreak.6 Although EMCV isolation was obtained from spleen, kidney, liver, whole blood, and heart, histopathologic lesions were confined to the cardiovascular system. No immunohistochemistry was performed on the organs submitted in our case. Immunohistochemistry could have emphasized that EMCV is principally cardiotropic in elephants, as it was previously reported for nonhuman primates.2,7
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This fatal case occurred in October, which is consistent with previous reports suggesting seasonality of the infection, typically reported during cold months.1,2 This seasonality is often linked to the behavior of rats looking for food and warmth in animals’ premises during cold months; as a result, there is a greater chance of contamination of food and water by their feces and urine. Pest control is performed on a regular basis in the receiving institution where the elephant died. Nevertheless, rodents are often seen in the elephants’ premises. Other elephants present at the time of death or previously held in this institution never presented with an EMCV infection to the authors’ knowledge. The death of this elephant occurred about 1 mo after her arrival at a new institution. The stress produced by the transport and the introduction to a new environment and bull could have lead to mild immunodeficiency and precipitated a fatal EMCV infection. Another differential diagnosis was toxic plant ingestion. Oleander (Nerium oleander, family Apocynaceae) is described as a potentially poisonous plant in elephants.4 Although this shrub was common throughout the zoo’s grounds, elephants do not have access to this plant in their enclosure, and zookeepers are aware of this threat, so plant toxicity was ruled out. Nevertheless, a complete exclusion of this hypothesis would have required a search for the toxins in the intestinal content. Other causes of sudden death in elephants include shock after bacterial or viral infections, such as EEHV infection.1,4 This report describes a fatal case of EMCV infection in an African elephant held in a French institution. To the authors’ knowledge, this is the first EMCV case in a captive African elephant in Europe. This confirms the risk of this virus in captive collections in Europe and the susceptibility of elephants to this virus. Thus, EMCV should be included in the differential diagnosis of sudden death in this species, particularly when myocarditis is observed or suspected at postmortem examination. Rodents are considered the source
of EMCV, and this emphasizes the necessity of pest control in captive collections.
LITERATURE CITED 1. Backues KA. Encephalomyocarditis virus infection in zoo animals. In: Fowler ME, Miller RE (eds.). Zoo and wild animal medicine—current therapy. 6th ed. St. Louis (MO): Saunders Elsevier; 2008. p. 75–78. 2. Canelli E, Luppi A, Lavazza A, Lelli D, Sozzi E, Moreno Martin AM, Gelmetti D, Pascotto E, Sandri C, Magnone W, Cordioli P. Encephalomyocarditis virus infection in an Italian zoo. Virol J. 2010;7:64. 3. Caroci M, Bakkali-Kassimi L. The encephalomyocarditis virus. Virulence. 2012;3:351–367. 4. Fowler ME, Mikota S. Biology, medicine and surgery of elephants. Ames (IA): Blackwell Publishing; 2006. 565 p. 5. Gaskin JM, Jorge MA, Simpson CF, Lewis AL, Olson JH, Schobert FE, Wollenman EP, Marlowe C, Curtis MM. The tragedy of encephalomyocarditis virus infection in zoological parks in Florida. Proc Am Assoc Zoo Vet. 1980;1–7. 6. Grobler DG, Raath JP, Braack LE, Keet DF, Gerdes GH, Barnard BJ, Kriek NP, Jardine J, Swanepoel R. An outbreak of encephalomyocarditis-virus infection in free-ranging African elephants in the Kruger National Park. Onderstepoort J Vet. 1995;62: 97–108. 7. La Rue R, Myers S, Brewer L, Shaw DP, Brown C, Seal BS, Njenga MK. A wild-type porcine encephalomyocarditis virus containing a short poly(C)tract is pathogenic to mice, pigs and Cynomologus macaques. J Virol. 2003;77:9136–9146. 8. MacLachlan NJ, Zee YC, Scott JL. Picornaviridae. In: Hirsh DC, MacLachlan NJ, Walker RL (eds.). Veterinary microbiology, 2nd ed. Ames (IA): Blackwell Publishing; 2004. p. 339–345. 9. Reddacliff LA, Kirkland PD, Hartley WJ, Reece RL. Encephalomyocarditis infections in an Australian zoo. J Zoo Wildl Med. 1997;28:153–157. 10. Simpson CF, Lewis AL, Gaskin JM. Encephalomyocarditis virus infection of captive elephants. J Am Vet Med Assoc. 1977;171:902–905. 11. Wells SK, Gutter AE, Soike KF, Baskin GB. Encephalomyocarditis virus: epizootic in a zoological collection. J Zoo Wildl Med. 1989;20:291–296. Received for publication 1 July 2014
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Zoo and Wildlife Medicine 46(2): 393–396, 2015 Copyright 2015 by American Association of Zoo Veterinarians
FATAL ENCEPHALOMYOCARDITIS VIRUS INFECTION IN AN AFRICAN SAVANNA ELEPHANT (LOXODONTA AFRICANA) IN A FRENCH ZOO Benjamin Lamglait, D.V.M., M.Sc., Antoine Joris, D.V.M., Aurore Romey, Labib Bakkali-Kassimi, Ph.D., and Karin Lemberger, D.V.M., Dipl. A.C.V.P.
Abstract: A fatal case of encephalomyocarditis virus (EMCV) involving an African elephant (Loxodonta africana) occurred in November 2013 at the Re´serve Africaine de Sigean, France. An adult female was found dead without any preliminary symptoms. Gross pathologic changes consisted of petechiae and hemorrhages on mucosae and internal organs, abundant transudate in the abdominal and pericardial cavities, and myocarditis. Histopathologic examination showed extensive degeneration and necrosis of ventricular cardiomyocytes with concurrent lymphoplasmocytic and eosinophilic infiltrate. An EMCV was isolated from several organs and considered the causative agent of the myocarditis. The same strain of virus was also isolated in rodents captured on zoo premises and considered to be the reservoir of the virus. To the authors’ knowledge, this is the first EMCV case in a captive African elephant in Europe. Key words: African elephant, death, encephalomyocarditis, Loxodonta africana, virus, zoo.
BRIEF COMMUNICATION The encephalomyocarditis virus (EMCV), genus Cardiovirus, family Picornaviridae, is a small nonenveloped, positive, single-stranded RNA virus that was first described in 1945. This virus is the causative agent of myocarditis and encephalitis but could also be responsible for reproductive disorders or diabetes in many mammalian species.1,3 The virus has an extremely broad host range, occurring in murid rodents, domestic and wild pigs, humans, and various captive species.1–3,5,8 Several outbreaks of fatal EMCV infections have been described in zoos in Australia, the United States, Italy, and Singapore.2,5,9–11 Sudden death was often the first indication of infection and was associated with acute fatal myocarditis. Although disease transmission is poorly understood, rodents are considered to be natural hosts of EMCV and thought to be the primary reservoir of the virus that might introduce and spread the virus by their infected carcasses or feces. These vectors contaminate feed and water, spreading the disease to susceptible animals.1,8
From the Re´serve Africaine de Sigean, 19 Chemin du hameau du lac, 11130 Sigean, France (Lamglait, Joris); UMR 1161 Virologie (Anses, Inra, Enva), ANSES–Laboratoire de Sante´ animale, 23 Avenue du Ge´ne´ral De Gaulle, 94700 Maisons-Alfort, France (Romey, Bakkali-Kassimi); and Vet Diagnostics, 14 Avenue Rockefeller, 69008 Lyon, France (Lemberger). Correspondence should be directed to Dr. Benjamin Lamglait ([email protected]).
This report describes the first EMCV infection in an African elephant (Loxodonta africana) housed in a French zoo. This case is described from a clinical, pathologic, and diagnostic point of view. Epidemiology and the role of rodents are also discussed. In November 2013, Seronga—an 18-yr-old wild-born female African elephant—was found dead without any preliminary symptoms. This individual had been transferred 1 mo before from a German zoo to the French institution at Sigean. She had adapted well to her new environment, though she appeared a bit more cautious than the other female that traveled with her. She was found dead in the morning, and the video recordings of the night revealed that she was active and ate with her cagemate until 6.00 AM, when she suddenly fell down. A full postmortem examination was performed. The main lesions consisted of petechiae and hemorrhages on the oral, ocular, rectal, and vaginal mucosae and on numerous internal organs such as spleen, heart, lymph nodes, large vessel walls, and mesovarium. There was also a marked cyanosis of her tongue, and a marked pulmonary congestion and edema. Abundant transudate was found in the abdominal cavity (about 100 L) and the pericardial cavity (about 20 L). Acute cardiac insufficiency was suspected. Some grey to white necrotic foci were seen in the myocardium, as well as petechiae and ecchymoses on the epicardial surface (Fig. 1). Because of the unspecific nature of the lesions observed, there are several differential diagnoses, including septicemia, viral infec-
393
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JOURNAL OF ZOO AND WILDLIFE MEDICINE
Figure 1. Petechiae and hemorrhages on oral mucosa and marked cyanosis of the tongue on an African elephant dead of EMCV infection. (Copyright B. Lamglait)
tion (elephant endotheliotrophic herpesvirus or encephalomyocarditis virus), or plant toxicity (mainly oleander). No clinical signs were noted on the other two African elephants held at the same institution. Bacteriology performed on several organs showed low quantities of nonspecific bacterial growth: Escherichia coli on the lungs and liver, considered contaminants; Pseudomonas aeruginosa on the trachea, also considered a contaminant because this bacteria is plant growth–promoting and no microscopic lesion was associated. The most significant lesions revealed by histopathology were extensive degeneration and necrosis of ventricular cardiomyocytes, with minimal infiltration by lymphocytes, macrophages, and fewer eosinophils and neutrophils (Fig. 2). Large areas of acute hemorrhages were noted in the adjacent epicardial adipose tissue and myocardium. Marked diffuse congestion and occasional hemorrhages and thrombosis were noted in other organs. The inflammatory microscopic lesions detected in the myocardium were consistent with an infectious etiology, particularly with a cardiovirus infection. For the virologic investigations, several tissues were tested by polymerase chain reaction (PCR) for elephant endotheliotropic herpesvirus (EEHV) 1–6, and all were negative. EMCV was detected by real-time reverse transcription (RT)PCR in the heart, kidney, and liver. The virus was
isolated on BHK-21 cells from the same organs and from blood and confirmed by sequencing. The death of this female African elephant occurred 1 mo after her arrival at Sigean. The transfer involved four females: two females were exchanged with two other females between Erfurt (Germany) and Sigean (France). Because the incubation period of EMCV is considered to be 9–45 days in rodents and pigs, a serological investigation was performed on all the females present in both institutions to determine where Seronga became infected. Only the two females from Sigean were positive for EMCV before the exchange. Another female who stayed at Erfurt had not seroconverted. Moreover, the EMCV serum neutralization test for Seronga was negative on the day of her death, demonstrating a recent infection. These findings suggest that the infection occurred at Sigean. Serum samples of elephants previously kept in Sigean were also tested to determine when the virus was present at the institution; it appears that EMCV has been present in Sigean since 2009. Because rodents are supposed to be the reservoir for EMCV, pest control was intensified. Additional traps were placed in the elephants’ premises to reduce the rodent population. Furthermore, food leftovers were systematically removed to avoid attracting rodents or contamination by their fomites. Mesenteric lymph node, sections of ileum, and feces from dead rats were collected for RT-PCR.
LAMGLAIT ET AL.—FATAL EMCV INFECTION IN AN AFRICAN ELEPHANT
395
Figure 2. Histological findings on the myocardium of an African elephant dead of EMCV infection. H&E. (A) Necrosis of cardiomyocytes, 340 magnification. (B) Necrosis of cardiomyocytes with inflammation associated, 3400 magnification. (Courtesy of K. Lemberger)
EMCV was detected by real-time RT-PCR in feces of 6/21 (28.6%) rats, in mesenteric lymph nodes of 4/19 (21.1%) rats (Rattus norvegicus), and in ileum sections of 2/21 (2.5%) rats. Serum was also used to perform immunofluorescence assays for antibody detection. Of the 13 rats tested, 3 (23%) were positive and 2 more were equivocal. A literature review revealed numerous reports describing encephalomyocarditis virus (EMCV) as the etiological agent of viral myocarditis in free-ranging and captive exotic mammals. Primates seem to be affected worldwide and include lemurs (Eulemur spp., Lemur spp., and Varecia spp.), marmosets (Callithrix jacchus), squirrel monkeys (Saimiri boliviensis), macaques (Macaca sylvanus), baboons (Papio spp.), gibbons (Hylobates spp.), orangutans (Pongo pygmaeus), chimpanzees (Pan troglodytes), and bonobos (Pan paniscus).1,2,7,9,11 EMCV infection was also implicated in the death of various animals at Audubon Park Zoo, New Orleans, in 1985, including a Thomson’s gazelle (Eudorcas thompsonii) and a dromedary camel (Camelus dromedarius).1,11 Sporadic outbreaks of EMCV have occurred in Taronga Zoo, Australia, from 1987 to 1995, involving primates, a pigmy hippopotamus (Hexaprotodon liberiensis) and two Goodfellows tree-kangaroos (Dendrolagus goodfellowi).9 Fatal cases of encephalomyocarditis infections were described in four captive African elephants
held in two zoos in Florida in 1977;10 outbreaks of EMCV in the United States have been primarily restricted to the southeastern states, where they have been described in eight zoos in six states.4 An outbreak of EMCV occurred in Kruger National Park, South Africa, between 1993 and 1994 and was responsible for the deaths of 64 free-ranging adult African elephants.6 Most of them (83%) were adult bulls. As reported in our case, the most common clinical presentation was sudden death, or only mild unspecific clinical signs associated with congestive heart failure. Gross pathology described in several case reports consist of excessive pericardial fluid, epicardial hemorrhages, and pale foci within the myocardium. Microscopic changes include myofiber necrosis, edema, and mononuclear cell infiltration within the myocardium.2,9,11 Nevertheless, not all infections in elephants result in clinical disease, as shown by the prevalence of EMCV seropositivity in elephants in the Kruger National Park after the 1993–1994 EMCV outbreak.6 Although EMCV isolation was obtained from spleen, kidney, liver, whole blood, and heart, histopathologic lesions were confined to the cardiovascular system. No immunohistochemistry was performed on the organs submitted in our case. Immunohistochemistry could have emphasized that EMCV is principally cardiotropic in elephants, as it was previously reported for nonhuman primates.2,7
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JOURNAL OF ZOO AND WILDLIFE MEDICINE
This fatal case occurred in October, which is consistent with previous reports suggesting seasonality of the infection, typically reported during cold months.1,2 This seasonality is often linked to the behavior of rats looking for food and warmth in animals’ premises during cold months; as a result, there is a greater chance of contamination of food and water by their feces and urine. Pest control is performed on a regular basis in the receiving institution where the elephant died. Nevertheless, rodents are often seen in the elephants’ premises. Other elephants present at the time of death or previously held in this institution never presented with an EMCV infection to the authors’ knowledge. The death of this elephant occurred about 1 mo after her arrival at a new institution. The stress produced by the transport and the introduction to a new environment and bull could have lead to mild immunodeficiency and precipitated a fatal EMCV infection. Another differential diagnosis was toxic plant ingestion. Oleander (Nerium oleander, family Apocynaceae) is described as a potentially poisonous plant in elephants.4 Although this shrub was common throughout the zoo’s grounds, elephants do not have access to this plant in their enclosure, and zookeepers are aware of this threat, so plant toxicity was ruled out. Nevertheless, a complete exclusion of this hypothesis would have required a search for the toxins in the intestinal content. Other causes of sudden death in elephants include shock after bacterial or viral infections, such as EEHV infection.1,4 This report describes a fatal case of EMCV infection in an African elephant held in a French institution. To the authors’ knowledge, this is the first EMCV case in a captive African elephant in Europe. This confirms the risk of this virus in captive collections in Europe and the susceptibility of elephants to this virus. Thus, EMCV should be included in the differential diagnosis of sudden death in this species, particularly when myocarditis is observed or suspected at postmortem examination. Rodents are considered the source
of EMCV, and this emphasizes the necessity of pest control in captive collections.
LITERATURE CITED 1. Backues KA. Encephalomyocarditis virus infection in zoo animals. In: Fowler ME, Miller RE (eds.). Zoo and wild animal medicine—current therapy. 6th ed. St. Louis (MO): Saunders Elsevier; 2008. p. 75–78. 2. Canelli E, Luppi A, Lavazza A, Lelli D, Sozzi E, Moreno Martin AM, Gelmetti D, Pascotto E, Sandri C, Magnone W, Cordioli P. Encephalomyocarditis virus infection in an Italian zoo. Virol J. 2010;7:64. 3. Caroci M, Bakkali-Kassimi L. The encephalomyocarditis virus. Virulence. 2012;3:351–367. 4. Fowler ME, Mikota S. Biology, medicine and surgery of elephants. Ames (IA): Blackwell Publishing; 2006. 565 p. 5. Gaskin JM, Jorge MA, Simpson CF, Lewis AL, Olson JH, Schobert FE, Wollenman EP, Marlowe C, Curtis MM. The tragedy of encephalomyocarditis virus infection in zoological parks in Florida. Proc Am Assoc Zoo Vet. 1980;1–7. 6. Grobler DG, Raath JP, Braack LE, Keet DF, Gerdes GH, Barnard BJ, Kriek NP, Jardine J, Swanepoel R. An outbreak of encephalomyocarditis-virus infection in free-ranging African elephants in the Kruger National Park. Onderstepoort J Vet. 1995;62: 97–108. 7. La Rue R, Myers S, Brewer L, Shaw DP, Brown C, Seal BS, Njenga MK. A wild-type porcine encephalomyocarditis virus containing a short poly(C)tract is pathogenic to mice, pigs and Cynomologus macaques. J Virol. 2003;77:9136–9146. 8. MacLachlan NJ, Zee YC, Scott JL. Picornaviridae. In: Hirsh DC, MacLachlan NJ, Walker RL (eds.). Veterinary microbiology, 2nd ed. Ames (IA): Blackwell Publishing; 2004. p. 339–345. 9. Reddacliff LA, Kirkland PD, Hartley WJ, Reece RL. Encephalomyocarditis infections in an Australian zoo. J Zoo Wildl Med. 1997;28:153–157. 10. Simpson CF, Lewis AL, Gaskin JM. Encephalomyocarditis virus infection of captive elephants. J Am Vet Med Assoc. 1977;171:902–905. 11. Wells SK, Gutter AE, Soike KF, Baskin GB. Encephalomyocarditis virus: epizootic in a zoological collection. J Zoo Wildl Med. 1989;20:291–296. Received for publication 1 July 2014
