Elsevier

Veterinary Microbiology

Volume 227, December 2018, Pages 143-147
Veterinary Microbiology

Multiple bluetongue virus serotypes causing death in Brazilian dwarf brocket deer (Mazama nana) in Brazil, 2015–2016

https://doi.org/10.1016/j.vetmic.2018.10.018Get rights and content

Highlights

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    Five different BTV serotypes were detected in Brazilian dwarf brocket deer (Mazama nana).

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    Serotypes 3, 14, 18, 19, 22 were isolated from animals with hemorrhagic disease.

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    Brazilian dwarf brocket deer (Mazama nana) is highly susceptible to BTV infection.

Abstract

Bela Vista Biological Sanctuary (RBV) is a protected area of Itaipu Binacional, a hydroelectric power company located on the border of Brazil and Paraguay. A captive population of Brazilian dwarf brocket deer (Mazama nana, Cervidae, Artiodactyla) is maintained for conservation purposes. Despite the reproductive success of the animals, outbreaks of a fatal hemorrhagic disease have been registered over the years, compromising conservation efforts. In order to identify the etiological agents of these hemorrhagic diseases, 32 captive Brazilian dwarf brockets were sampled to investigate bluetongue virus (BTV), epizootic hemorrhagic disease (EHD), and adenovirus hemorrhagic disease (AHD), in 2015. Only one deer (1/32; 3.12%) was seropositive for BTV. After this survey, five animals died in the early autumn of 2015 and 2016, again presenting clinical signs of hemorrhagic disease. Using RT-qPCR, RT-PCR and DNA sequencing, five BTV serotypes (3, 14, 18, 19, and 22) were identified in blood and tissues collected during necropsies. These BTV serotypes had not been previously described or isolated in Brazil, either in wild or domestic ruminants. Additionally, differential diagnosis was performed for EHD and AHD, but all samples were negative for both diseases. The multiple distinct BTV serotypes identified in these outbreaks resulted in a high lethality (100%) of Brazilian dwarf brockets and indicated that various BTV serotypes are circulating in the area.

Introduction

Brazil has a great diversity of deer species, with eight species currently recognized, from which at least three (Mazama nana, Mazama bororo, and Blastocerus dichotomus) have vulnerable conservation status (IUCN, 2017). Despite the reproductive success of breeding centers and zoos over the years, the mortality rate is still high due to different diseases. Hemorrhagic disorders are among the most common diseases of deer raised in captivity in Brazil (Werther and Kawanami, 2014). Adenovirus hemorrhagic disease (AHD), epizootic hemorrhagic disease (EHD), and bluetongue (BT) are generally associated with hemorrhagic infection diseases in deer. AHD is caused by Deer Atadenovirus A (AHDV), recently recognized as a new species in the Atadenovirus genus, Adenoviridae family (Miller et al., 2017) and so far, there are no reports of hemorrhagic disease in deer caused by adenovirus in South America. The epizootic hemorrhagic disease virus (EHDV) and bluetongue virus (BTV) belong to the genus Orbivirus within the Reoviridae family, these viruses are transmitted by Culicoides sp. midges and their occurrence corresponds to the vector distribution, which is widespread in tropical and subtropical zones of the planet (Mellor et al., 2000). To date, at least 27 BTV and seven EHDV serotypes have been recognized, with distinct occurrences around the world (Maan et al., 2012; Maclachlan et al., 2015; Schulz et al., 2016).

Itaipu Binacional is a hydroelectric power company located at the boundary between Brazil and Paraguay, Paraná River basin. The Bela Vista Biological Sanctuary (CASIB) is a protected area of 1920 ha in Foz do Iguaçu, Paraná State, Brazil, managed by Itaipu Binacional. Itaipu Binacional is the holder of the largest captive herd of Mazama nana, and successful reproduction of the species happens continuously in this location, but cases of hemorrhagic disease of uncertain etiology have led to the deaths of a considerable number of animals over the years, compromising conservation efforts. Hemorrhagic syndrome was first observed during necropsy of captive deer at the CASIB in 1990; subsequently, necropsy reports from 1995, 1997, 1998, 2003, 2004, and from 2008 to 2016 described pathological findings compatible with hemorrhagic disease. Over the years, four species of native cervids (M. nana, M. gouazoubira, M. americana, and B. dichotomus) were affected by hemorrhagic disease. In this study, we investigate the possible viral agents involved in the etiology of hemorrhagic disease outbreaks in deer, which occurred in 2015 and 2016 at CASIB.

Section snippets

Ethics

This study was approved by the Ethics Committee and Animal Welfare – CETEA from Universidade Estadual de Santa Catarina, according to protocol 01.70.14, and the SISBIO authorization number of the study is 50068-1. The World Organization for Animal Health (OIE) and Ministry of Agriculture, Livestock and Food Supply, Brazil were notified of the results of this study.

Animal sampling

As a part of a research project investigating hemorrhagic diseases occurring in CASIB in the last 16 years, between February and

Results

Of the 32 deer tested before the beginning of the 2015 hemorrhagic disease outbreak, only one (3.12%) was positive by AGID for BTV, indicating a high number of seronegative animals. The blood samples collected from these asymptomatic animals were all negative for BTV, EHDV and AHV by molecular diagnostic testing, indicating no evidence of these viruses’ circulation in the herd at that point in time. However, a number of weeks after the blood sampling, four animals died in CASIB, presenting

Discussion

The serological survey by the AGID method revealed a low prevalence of BTV seropositive animals (3.12%; 1/32). The low antibody prevalence, in addition to the history of hemorrhagic disease causing deaths in the herd of deer in CASIB, may suggest that those animals were highly susceptible to BTV infection, such that only a small number of animals survive the infection long enough to produce antibodies against the virus. To support this affirmation, AGID testing performed on serum samples from

Conclusion

Although recurrent hemorrhagic disease outbreaks leading to deer mortality have been registered at the Bela Vista Biological Refuge since 1990, studies of the causative agents in domestic, and especially wild ruminants, are very scarce in Brazil. The OIE have been notified of these BTV outbreaks and the identification of the serotypes associated with the outbreaks. The identification of serotypes occurring in Brazil is essential for disease epidemiology studies. Moreover, molecular and

Conflict of interest statement

There are no potential conflicts (financial, professional, or personal) that are relevant to the manuscript.

Funding

This research did not receive any specific grants from funding agencies in the public, commercial, or not-for-profit sectors.

Acknowledgments

We are very thankful to Prof. Peter Mertens and Dr. Kyriaki Nomikou for sharing their wealth of knowledge regarding orbiviruses. This study was supported by Itaipu Binacional, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Grant PVE 185/2012). Z. I.P. Lobato has a CNPq fellowship.

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