Two common forms of equine herpesvirus which cause respiratory disorders, abortion and occasionally neurological disease in horses appear to have evolved a broad range of hosts among African mammals, researchers report.
The international team of researchers set out to determine the true extent of the host range of equine herpesvirus type 1 (EHV-1) and equine herpevirus type 9 (EHV-9).
The scientists, writing in the open-access journal, PLOS ONE, said that a range of animals other than horses showed evidence of having been exposed to one or both of the viruses, in some cases carrying antibodies against them.
Alex Greenwood and his colleagues said EHV-1 and EHV-9 were somewhat unusual herpesviruses and lacked strict host specificity. “The true extent of their host ranges have remained unclear,” they noted.
The researchers tested a total of 428 serum samples from captive and wild animals, representing 30 species in 12 families and five orders.
They found that equidae, rhinoceros species, and some members of the bovidae family – the diverse group of ungulates that includes antelope, sheep, goats, cattle, buffalo, and bison – were serologically positive for EHV-1 and EHV-9.
They found that the prevalence of EHV-1 in the sampled wild zebra populations was significantly higher than in zoos, suggesting captivity may reduce exposure to EHV-1. Furthermore, the prevalence for EHV-1 in the samples was significantly higher than for EHV-9 in zebras.
In contrast, EHV-9 antibody prevalence was high in captive and wild African rhinoceros species, suggesting that they may serve as a reservoir or natural host for EHV-9.
“Thus, EHV-1 and EHV-9 have a broad host range favoring African herbivores and may have acquired novel natural hosts in ecosystems where wild equids are common and are in close contact with other perissodactyls [odd-toed ungulates],” the study team reported.
The researchers noted that nine herpesviruses had been identified among equidae.
EHV-1, they said, was arguably one of the most important equine pathogens, with a worldwide distribution in domestic horses, causing respiratory disease, abortion, neonatal death and neurological disorders.
Infections with EHV-1 or closely related viruses have been identified in other equids, including zebras, domestic donkeys, and onagers. EHV-1 infection has previously been reported in the Indian tapir (Tapirus indicus) and the black rhinoceros (Diceros bicornis). EHV-1 antibodies were detected with a prevalence of 8.8% in African white (Ceratotherium simum) and black (Diceros bicornis) rhinoceroses.
EHV-9, they said, was first described in captive Thomson’s gazelle in Japan that suffered from neurological symptoms and died, but were considered an accidental host.
Neither the natural host nor the complete host range of EHV-9 was yet known, but it was known to cause lethal disease in several different species under experimental conditions.
Both EHV-1 and/or EHV-9 have been shown to infect species in captivity other than their known natural hosts, resulting in disease and fatalities in species such as polar bear, black bear, llamas, alpacas, blackbuck antelope, Thomson’s gazelle, and giraffe.
“The complete host range of EHV-1 and EHV-9 and whether there are differences in captivity that potentially promote cross-species transmission remains unknown,” the scientists said.
For their research, 277 serum samples were collected from a range of captive non-vaccinated animals across 43 zoos and 151 samples from free-ranging species in Tanzania and Namibia.
Of 132 serum samples from equids in captivity, 60 were seropositive for EHV-1 and 59 were seropositive for EHV-9. Among the 41 wild plains zebra serum samples, 32 were positive for EHV-1 and and 35 for EHV-9.
The 12 samples collected from captive kiangs, onagers or ponies were negative for antibodies against both viruses, they said.
Out of 64 captive white rhinoceros samples, 9 were were seropositive for EHV-1 and 26 for EHV-9 antibodies.
The six samples from captive black rhinoceroses did not show neutralizing antibodies against EHV-1 or EHV-9. But in 17 wild black rhinoceros samples, one was positive for EHV-1 antibodies and two for EHV-9 antibodies.
Overall, they found evidence of significant previous exposure among the rhinoceros samples.
None of the tested captive or wild non-equid samples tested positive for either virus, except for one captive lesser kudu antelope.
They found no neutralizing antibodies for either EHV-1 or EHV-9 in any of the tested carnivore serum samples – 16 of which were from captive animals and 41 from wild ones.
Four donkeys among the 12 tested were found to be positive for EHV-1 antibodies. In Somali wild asses, 14 of the 19 samples were positive for EHV-1 antibodies and one was positive for EHV-9 antibodies.
“The prevalence of EHV-1 antibodies in the tested plains zebra (wild or captive), captive Hartmann’s zebra, and captive Somali wild ass sera was significantly higher than that of EHV-9,” they noted.
The researchers noted that none of the animals tested, wild or captive, were found to have displayed clinical signs associated with herpesvirus infection.
“This is characteristic of natural viral host species and may be suggestive of co-adaptation of species that are natural conspecifics of equid reservoir animals.”
They said the unexpectedly high prevalence of EHV-9 antibodies in rhinoceroses – particularly captive white rhinos – suggested they were susceptible to EHV-9 infection and may serve as a natural and possibly definitive host or reservoir.
“The question of the natural reservoir and definitive host is particularly important for EHV-9 as the source of the many fatal infections of ungulates under natural conditions was not identified.
“Both EHV-1 and EHV-9 have been involved in fatal encephalitis cases in captive polar bears without proximity to equids. Rhinoceroses, which were not considered a potential source of infection, may have been involved in these unexplained transmission events,” they said.
“Similarly, a recent Asian rhinoceros fatality as a consequence of EHV-1 infection was suspected from a zebra source but may have derived from an African rhinoceros.”
The researchers noted that mammals in many African ecosystems congregated at water sources during periods of seasonal water shortage, which may explain the transmission of viruses among animals.
They said the low prevalence of EHV-9-positive antelopes supported the hypothesis that these species were accidental hosts of the virus.
They noted that carnivores could be infected with EHV-1 and/or EHV-9 experimentally, causing neurological disease and death.
“Our findings suggest that carnivores are less frequently infected by EHV or fail to seroconvert and, based on experimental infection, may be more likely to exhibit neurological symptoms when infection does occur.
“African carnivores, many of which prey on or scavenge equids, may have evolved resistance to EHV as a result of the high risk of exposure to infection,” the authors suggested.
“Polar bears and non-African carnivores would not be expected to have evolved such resistance, which may explain the relatively frequent observed fatal disease in species that are not naturally sympatric with African perissodactyls.”
They continued: “Taken together, we propose that EHV-1 and EHV-9 have evolved a broad host range among African mammals …
“The results presented here show that different families including Equidae, Rhinocerotidae and Bovidae, respond with robust antibody responses to EHV-1 and EHV-9 exposure.
“The high prevalence in the Rhinoceroteridae in particular, suggests that they may be a natural host and/or reservoir for EHV-9. Further study is needed to determine the role of these animals in EHV epidemiology in both captivity and the wild.”
Greenwood was joined in the research by Azza Abdelgawad, Robert Hermes, Armando Damiani, Benjamin Lamglait, Gábor Á. Czirják, Marion East, Ortwin Aschenborn, Christian Wenker, Samy Kasem and Nikolaus Osterrieder.
Abdelgawad A, Hermes R, Damiani A, Lamglait B, Czirják GÁ, East M, et al. (2015) Comprehensive Serology Based on a Peptide ELISA to Assess the Prevalence of Closely Related Equine Herpesviruses in Zoo and Wild Animals. PLoS ONE 10(9): e0138370. doi:10.1371/journal.pone.0138370
The full study can be read here.