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      Abortive vampire bat rabies infections in Peruvian peridomestic livestock

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          Abstract

          Rabies virus infections normally cause universally lethal encephalitis across mammals. However, ‘abortive infections’ which are resolved prior to the onset of lethal disease have been described in bats and a variety of non-reservoir species. Here, we surveyed rabies virus neutralizing antibody titers in 332 unvaccinated livestock of 5 species from a vampire bat rabies endemic region of southern Peru where livestock are the main food source for bats. We detected rabies virus neutralizing antibody titers in 11, 5 and 3.6% of cows, goats and sheep respectively and seropositive animals did not die from rabies within two years after sampling. Seroprevalence was correlated with the number of local livestock rabies mortalities reported one year prior but also one year after sample collection. This suggests that serological status of livestock can indicate the past and future levels of rabies risk to non-reservoir hosts. To our knowledge, this is the first report of anti-rabies antibodies among goats and sheep, suggesting widespread abortive infections among livestock in vampire bat rabies endemic areas. Future research should resolve the within-host biology underlying clearance of rabies infections. Cost-effectiveness analyses are also needed to evaluate whether serological monitoring of livestock can be a viable complement to current monitoring of vampire bat rabies risk based on animal mortalities alone.

          Author summary

          Rabies virus is the deadliest virus affecting mammals. In Latin America, rabies transmitted by vampire bats is one of the most recognized zoonoses affecting humans and livestock. For unknown reasons, species such as bats and cattle can produce antibodies against rabies that clear viral infection prior to the development of deadly clinical signs. However, the extend of this phenomenon in naturally exposed populations remains unknows. In this study, we detected anti-rabies antibodies among cattle and, for the first time, goats and sheep bitten by vampire bats across as large geographic area endemic of vampire bat rabies in South Peru. We also showed that the presence of antibodies in livestock can indicate the past and future levels of cattle mortality due to rabies in the area. Future research should resolve the within-host biology underlying clearance of rabies infections and evaluate if antibody detection of healthy animals can be used for monitoring vampire bat rabies risk.

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          Most cited references29

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          Deciphering serology to understand the ecology of infectious diseases in wildlife.

          The ecology of infectious disease in wildlife has become a pivotal theme in animal and public health. Studies of infectious disease ecology rely on robust surveillance of pathogens in reservoir hosts, often based on serology, which is the detection of specific antibodies in the blood and is used to infer infection history. However, serological data can be inaccurate for inference to infection history for a variety of reasons. Two major aspects in any serological test can substantially impact results and interpretation of antibody prevalence data: cross-reactivity and cut-off thresholds used to discriminate positive and negative reactions. Given the ubiquitous use of serology as a tool for surveillance and epidemiological modeling of wildlife diseases, it is imperative to consider the strengths and limitations of serological test methodologies and interpretation of results, particularly when using data that may affect management and policy for the prevention and control of infectious diseases in wildlife. Greater consideration of population age structure and cohort representation, serological test suitability and standardized sample collection protocols can ensure that reliable data are obtained for downstream modeling applications to characterize, and evaluate interventions for, wildlife disease systems.
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            Prevalence of antibodies against Rift Valley fever virus in Kenyan wildlife.

            Rift Valley fever virus (RVFV) is an arbovirus associated with periodic outbreaks, mostly on the African continent, of febrile disease accompanied by abortion in livestock, and a severe, fatal haemorrhagic syndrome in humans. However, the maintenance of the virus during the inter-epidemic period (IEP) when there is low or no disease activity detected in livestock or humans has not been determined. This study report prevalence of RVFV-neutralizing antibodies in sera (n=896) collected from 16 Kenyan wildlife species including at least 35% that were born during the 1999-2006 IEP. Specimens from seven species had detectable neutralizing antibodies against RVFV, including African buffalo, black rhino, lesser kudu, impala, African elephant, kongoni, and waterbuck. High RVFV antibody prevalence (>15%) was observed in black rhinos and ruminants (kudu, impala, buffalo, and waterbuck) with the highest titres (up to 1:1280) observed mostly in buffalo, including animals born during the IEP. All lions, giraffes, plains zebras, and warthogs tested were either negative or less than two animals in each species had low ( or= 1:80. These data provide evidence that wild ruminants are infected by RVFV but further studies are required to determine whether these animals play a role in the virus maintenance between outbreaks and virus amplification prior to a noticeable outbreak.
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              Dynamics of a morbillivirus at the domestic-wildlife interface: Canine distemper virus in domestic dogs and lions.

              Morbilliviruses cause many diseases of medical and veterinary importance, and although some (e.g., measles and rinderpest) have been controlled successfully, others, such as canine distemper virus (CDV), are a growing concern. A propensity for host-switching has resulted in CDV emergence in new species, including endangered wildlife, posing challenges for controlling disease in multispecies communities. CDV is typically associated with domestic dogs, but little is known about its maintenance and transmission in species-rich areas or about the potential role of domestic dog vaccination as a means of reducing disease threats to wildlife. We address these questions by analyzing a long-term serological dataset of CDV in lions and domestic dogs from Tanzania's Serengeti ecosystem. Using a Bayesian state-space model, we show that dynamics of CDV have changed considerably over the past three decades. Initially, peaks of CDV infection in dogs preceded those in lions, suggesting that spill-over from dogs was the main driver of infection in wildlife. However, despite dog-to-lion transmission dominating cross-species transmission models, infection peaks in lions became more frequent and asynchronous from those in dogs, suggesting that other wildlife species may play a role in a potentially complex maintenance community. Widespread mass vaccination of domestic dogs reduced the probability of infection in dogs and the size of outbreaks but did not prevent transmission to or peaks of infection in lions. This study demonstrates the complexity of CDV dynamics in natural ecosystems and the value of long-term, large-scale datasets for investigating transmission patterns and evaluating disease control strategies.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: Methodology
                Role: MethodologyRole: Writing – review & editing
                Role: Methodology
                Role: Investigation
                Role: Methodology
                Role: Methodology
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                29 June 2020
                June 2020
                : 14
                : 6
                : e0008194
                Affiliations
                [1 ] Departamento de Ecología y Biodiversidad, Facultad de Ciencias de la Vida, Universidad Andrés Bello, Santiago, Chile
                [2 ] Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom
                [3 ] Centro de Investigación para la Sustentabilidad, Facultad de Ciencias de la Vida, Universidad Andrés Bello, Santiago, Chile
                [4 ] Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, NE, Atlanta, Georgia, United States of America
                [5 ] Colegio Médico Veterinario de Apurimac, Abancay, Peru
                [6 ] Association for the Conservation and Development of Natural Resources, Lima, Peru
                [7 ] Faculty of Veterinary Medicine and Zootechnics, Universidad Peruana Cayetano Heredia, Lima, Peru
                [8 ] MRC-University of Glasgow Centre for Virus Research, Sir Henry Wellcome Building, Glasgow, Scotland, United Kingdom
                International Atomic Energy Agency, AUSTRIA
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-3920-9165
                http://orcid.org/0000-0003-1538-9373
                http://orcid.org/0000-0001-7475-2705
                Article
                PNTD-D-19-01240
                10.1371/journal.pntd.0008194
                7351222
                32598388
                17833958-ee88-42be-be80-dacc571b5298

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 12 August 2019
                : 3 March 2020
                Page count
                Figures: 1, Tables: 1, Pages: 13
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 102507/Z/13/Z
                Award Recipient :
                DS and JB were funded by a Sir Henry Dale Fellowship, jointly funded by the Wellcome Trust and Royal Society (Grant 102507/Z/13/Z). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Biology and Life Sciences
                Agriculture
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                Biology and Life Sciences
                Organisms
                Eukaryota
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                Lyssavirus
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                2020-07-10
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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