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      Squirrelpox Virus: Assessing Prevalence, Transmission and Environmental Degradation

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          Abstract

          Red squirrels ( Sciurus vulgaris) declined in Great Britain and Ireland during the last century, due to habitat loss and the introduction of grey squirrels ( Sciurus carolinensis), which competitively exclude the red squirrel and act as a reservoir for squirrelpox virus (SQPV). The disease is generally fatal to red squirrels and their ecological replacement by grey squirrels is up to 25 times faster where the virus is present. We aimed to determine: (1) the seropositivity and prevalence of SQPV DNA in the invasive and native species at a regional scale; (2) possible SQPV transmission routes; and, (3) virus degradation rates under differing environmental conditions. Grey ( n = 208) and red ( n = 40) squirrel blood and tissues were sampled. Enzyme-linked immunosorbent assay (ELISA) and quantitative real-time polymerase chain reaction (qPCR) techniques established seropositivity and viral DNA presence, respectively. Overall 8% of squirrels sampled (both species combined) had evidence of SQPV DNA in their tissues and 22% were in possession of antibodies. SQPV prevalence in sampled red squirrels was 2.5%. Viral loads were typically low in grey squirrels by comparison to red squirrels. There was a trend for a greater number of positive samples in spring and summer than in winter. Possible transmission routes were identified through the presence of viral DNA in faeces (red squirrels only), urine and ectoparasites (both species). Virus degradation analyses suggested that, after 30 days of exposure to six combinations of environments, there were more intact virus particles in scabs kept in warm (25°C) and dry conditions than in cooler (5 and 15°C) or wet conditions. We conclude that SQPV is present at low prevalence in invasive grey squirrel populations with a lower prevalence in native red squirrels. Virus transmission could occur through urine especially during warm dry summer conditions but, more notably, via ectoparasites, which are shared by both species.

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          Most cited references14

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          Leptospirosis: a zoonotic disease of global importance.

          In the past decade, leptospirosis has emerged as a globally important infectious disease. It occurs in urban environments of industrialised and developing countries, as well as in rural regions worldwide. Mortality remains significant, related both to delays in diagnosis due to lack of infrastructure and adequate clinical suspicion, and to other poorly understood reasons that may include inherent pathogenicity of some leptospiral strains or genetically determined host immunopathological responses. Pulmonary haemorrhage is recognised increasingly as a major, often lethal, manifestation of leptospirosis, the pathogenesis of which remains unclear. The completion of the genome sequence of Leptospira interrogans serovar lai, and other continuing leptospiral genome sequencing projects, promise to guide future work on the disease. Mainstays of treatment are still tetracyclines and beta-lactam/cephalosporins. No vaccine is available. Prevention is largely dependent on sanitation measures that may be difficult to implement, especially in developing countries.
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            Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment.

            The capability of rodent-borne viruses to survive outside the host is critical for the transmission dynamics within rodent populations and to humans. The transmission of Puumala virus (PUUV) in colonized bank voles (Clethrionomys glareolus) was investigated and additional longevity studies in cell culture with PUUV and Tula (TULV) hantaviruses were performed. Wild-type PUUV excreted by experimentally infected donor bank voles was shown to be transmitted indirectly between rodents through contaminated beddings, and maintained its infectivity to recipient voles at room temperature for 12-15 days. In cell culture supernatants, PUUV and TULV remained infectious for 5-11 days at room temperature and up to 18 days at 4 degrees C, but were inactivated after 24 h at 37 degrees C. Interestingly, a fraction of dried virus was still infectious after 1 h at 56 degrees C. These results demonstrated that hantavirus transmission does not require direct contact between rodents, or between rodents and humans, and that the indirect transmission of PUUV through contaminated environment takes place among the rodents for a prolonged period of time. The results also have implications for safety recommendations for work with hantaviruses and for preventive measures.
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              Disease threats posed by alien species: the role of a poxvirus in the decline of the native red squirrel in Britain.

              Red squirrels are declining in the United Kingdom. Competition from, and squirrel poxvirus (SQPV) disease carried by, grey squirrels are assumed to be determining the decline. We analyse the incidence of disease and changes in distribution of the two species in Cumbria, from 1993 to 2003 and compare these to the predictions of an individual-based (IB) spatially explicit disease model simulating the dynamics of both squirrel species and SQPV in the landscape. Grey squirrels increased whilst red squirrels declined over 10 years. The incidence of disease in red squirrels was related to the time since grey squirrels arrived in the landscape. Analysis of rates of decline in red squirrel populations in other areas showed that declines are 17-25 times higher in regions where SQPV is present in grey squirrel populations than in those where it is not. The IB model predicted spatial overlap of 3-4 years between the species that was also observed in the field. The model predictions matched the observed data best when contact rates and rates of infection between the two species were low. The model predicted that a grey squirrel population control of >60% effective kill was needed to stop the decline in red squirrel populations in Cumbria.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                21 February 2014
                : 9
                : 2
                : e89521
                Affiliations
                [1 ]Quercus, School of Biological Sciences, Queen’s University Belfast, Belfast, Northern Ireland
                [2 ]School of Biological Sciences, Queen’s University Belfast, Belfast, Northern Ireland
                [3 ]Institute for Global Food Security (IGFS), Queen’s University Belfast, Belfast, Northern Ireland
                [4 ]School of Life Sciences, University of Lincoln, Lincolnshire, England
                [5 ]Moredun Research Institute, Penicuik, Midlothian, Scotland
                [6 ]Animal Health and Veterinary Laboratories Agency (AHVLA), Addlestone, Surrey, England
                USGS National Wildlife Health Center, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LMC CM DE WIM MS NM JTAD NR. Performed the experiments: NDW DT CM DE. Analyzed the data: LMC NDW NR. Wrote the paper: LMC NDW DT CM DE WIM MS NM JTAD NR.

                Article
                PONE-D-13-36474
                10.1371/journal.pone.0089521
                3931809
                5bfe6e34-9320-4551-9543-557519125e81
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 4 September 2013
                : 21 January 2014
                Page count
                Pages: 8
                Funding
                This project was part-funded by the Natural Heritage Research Partnership (NHRP) between the Northern Ireland Environment Agency (NIEA) and Quercus, Queen’s University Belfast (QUB) and part-funded by the People’s Trust for Endangered Species (PTES) conducted in collaboration with the Moredun Research Institute and the Animal Health and Veterinary Laboratories Agency (AHVLA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Conservation science
                Population biology
                Epidemiology
                Infectious disease epidemiology
                Zoology
                Mammalogy
                Veterinary science
                Animal types
                Wildlife
                Veterinary diseases
                Veterinary parasitology
                Veterinary virology
                Veterinary epidemiology

                Uncategorized
                Uncategorized

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