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      Susceptibility of spotted doves ( Streptopelia chinensis) to experimental infection with the severe fever with thrombocytopenia syndrome phlebovirus

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          Abstract

          Background

          Severe fever with thrombocytopenia syndrome virus (SFTSV), an emerging human pathogen naturally transmitted by ticks, has spread widely since it was first detected in 2010. Although SFTSV-specific antibodies have been detected in wild birds, these natural reservoir and amplifying hosts for the virus have not been well studied.

          Methodology/Principle findings

          Here we report an experimental infection of spotted doves ( Streptopelia chinensis) with two strains of SFTSV, JS2010-14, a Chinese lineage strain, and JS2014-16, a Japanese lineage strain, which represent the main viral genotypes currently circulating in East Asia. In these studies, we have determined that spotted doves are susceptible to SFTSV and the severity of the viremia is dose-dependent. When challenged with 10 7 and 10 5 PFU, all doves developed viremia which peaked 3–5 days post infection (dpi). Only a subset (25–62.5%) of the birds developed viremia when challenged at 10 3 PFU. Virulence of SFTSV in spotted doves was strain dependent. Infection with 10 7 PFU of strain JS2014-16 resulted in 12.5% mortality over 6.8 days and mean peak viremia titers of 10 6.9 PFU/mL in experimentally inoculated birds. All doves inoculated with 10 7 PFU of the JS2010-14 strain survived infection with relatively lower mean viremia titers (10 5.6 PFU/mL at peak) over 6.1 days.

          Conclusions/Significance

          Our results suggest that spotted doves, one of the most abundant bird species in China, could be a competent amplifying host for SFTSV and play an important role in its ecology. Between the two SFTSV strains, the strain of the Japanese lineage caused mortality, higher viremia titers in infected birds over a longer time period than did the Chinese strain. Our observations shed light on the ecology of SFTSV, which could benefit the implementation of surveillance and control programs.

          Author summary

          Severe fever with thrombocytopenia syndrome virus (SFTSV) is an emerging human pathogen naturally transmitted by ticks. Our recent study has showed that some species of migratory birds, such as swan geese and spotted doves, can be parasitized by Haemaphysalis longicornis, an SFTSV vector, and antibodies against the SFTSV detected in these species. These data demonstrate that migratory birds are infected with SFTSV and may also play a role in the infection of ticks with SFTSV. Other studies have reported that migratory bird routes and the distribution of H. longicornis in East Asia overlap with the geographic distribution of SFTSV. Migratory birds are known to be carriers and transmitters of infectious agents, like the causative agents of influenza, West Nile encephalitis, and Lyme disease. Wild birds often travel long distances carrying various parasites, including ticks, which may be infected with viruses and bacteria. It is therefore reasonable to hypothesize that migratory birds may have played an important role in spreading SFTSV in two potential transmission scenarios: 1) birds are infected with the virus and transmit it back to ticks endemically or in a distal region, or 2) they are carriers of parasitic ticks that are infected with the virus. Here we report an experimental infection of spotted doves ( Streptopelia chinensis) with two strains of SFTSV, JS2010-14 from a Chinese lineage and JS2014-16 from a Japanese lineage, which represent the main viral genotypes currently circulating in East Asia. We determined that spotted doves are susceptible to SFTSV and that the severity of the viremia was dose and strain dependent. Infection with the strain of JS2014-16 led to a death rate of 12.5% and higher viremia titers in experimentally inoculated birds while doves inoculated with the JS2010-14 strain survived infection with relatively lower virus titers in the blood. These findings provide novel insights for understanding the rapid spread of the virus in a short time span, in particular the SFTSV strains from the Japanese lineage (genotype E).

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          Most cited references23

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          Pathogenesis of emerging severe fever with thrombocytopenia syndrome virus in C57/BL6 mouse model.

          The discovery of an emerging viral disease, severe fever with thrombocytopenia syndrome (SFTS), caused by SFTS virus (SFTSV), has prompted the need to understand pathogenesis of SFTSV. We are unique in establishing an infectious model of SFTS in C57/BL6 mice, resulting in hallmark symptoms of thrombocytopenia and leukocytopenia. Viral RNA and histopathological changes were identified in the spleen, liver, and kidney. However, viral replication was only found in the spleen, which suggested the spleen to be the principle target organ of SFTSV. Moreover, the number of macrophages and platelets were largely increased in the spleen, and SFTSV colocalized with platelets in cytoplasm of macrophages in the red pulp of the spleen. In vitro cellular assays further revealed that SFTSV adhered to mouse platelets and facilitated the phagocytosis of platelets by mouse primary macrophages, which in combination with in vivo findings, suggests that SFTSV-induced thrombocytopenia is caused by clearance of circulating virus-bound platelets by splenic macrophages. Thus, this study has elucidated the pathogenic mechanisms of thrombocytopenia in a mouse model resembling human SFTS disease.
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            Severe Fever with Thrombocytopenia Syndrome Virus in Ticks Collected from Humans, South Korea, 2013

            We investigated the infection rate for severe fever with thrombocytopenia syndrome virus (SFTSV) among ticks collected from humans during May–October 2013 in South Korea. Haemaphysalis longicornis ticks have been considered the SFTSV vector. However, we detected the virus in H. longicornis, Amblyomma testudinarium, and Ixodes nipponensis ticks, indicating additional potential SFTSV vectors.
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              Phylogenetic and Geographic Relationships of Severe Fever With Thrombocytopenia Syndrome Virus in China, South Korea, and Japan.

              Severe fever with thrombocytopenia syndrome (SFTS) is a tick-borne acute infectious disease caused by the SFTS virus (SFTSV). SFTS has been reported in China, South Korea, and Japan as a novel Bunyavirus. Although several molecular epidemiology and phylogenetic studies have been performed, the information obtained was limited, because the analyses included no or only a small number of SFTSV strains from Japan.
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                Author and article information

                Contributors
                Role: Funding acquisitionRole: MethodologyRole: Project administrationRole: Writing – original draft
                Role: ConceptualizationRole: Project administration
                Role: Formal analysisRole: Funding acquisition
                Role: ResourcesRole: Software
                Role: Software
                Role: Data curationRole: Resources
                Role: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: 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
                5 July 2019
                July 2019
                : 13
                : 7
                : e0006982
                Affiliations
                [1 ] Nanjing University Medical School and Jiangsu Provincial Key Laboratory of Medicine, Nanjing, China
                [2 ] Jiangsu Provincial Center for Disease Prevention and Control, Nanjing, China
                [3 ] College of Veterinary Medicine, University of Minnesota at Twin Cities, Saint Paul, Minnesota, United States of America
                Fort Collins, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Article
                PNTD-D-18-01717
                10.1371/journal.pntd.0006982
                6636776
                31276495
                75a4625e-6988-49aa-b1ef-e173d9052e14
                © 2019 Li et al

                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
                : 1 November 2018
                : 27 April 2019
                Page count
                Figures: 4, Tables: 1, Pages: 14
                Funding
                Funded by: National Nature Science Foundation of China
                Award ID: 81571993
                Award Recipient :
                Funded by: National Nature Science Foundation of China
                Award ID: 81703284
                Award Recipient :
                Funded by: National Nature Science Foundation of China
                Award ID: 81601794
                Award Recipient :
                Funded by: Jiangsu provincial Nature Science Foundation
                Award ID: BK20161584
                Award Recipient :
                This work was supported by grants from the National Nature Science Foundation of China ( http://www.nsfc.gov.cn) (Grant No. 81571993 to XZ; 81703284 to LZ and 81601794 to HJ). This work was also supported by a grant from Jiangsu provincial Nature Science Foundation ( http://kxjst.jiangsu.gov.cn/) (Grant No. BK20161584 to LZ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Medicine and Health Sciences
                Infectious Diseases
                Viral Diseases
                Viremia
                Biology and Life Sciences
                Psychology
                Behavior
                Animal Behavior
                Animal Migration
                Social Sciences
                Psychology
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                Medicine and Health Sciences
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                Biology and Life Sciences
                Biochemistry
                Proteins
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                Antibodies
                Medicine and Health Sciences
                Infectious Diseases
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                Ticks
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Ticks
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Arachnida
                Ixodes
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                Biology and Life Sciences
                Molecular Biology
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                Polymerase Chain Reaction
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                Research and Analysis Methods
                Molecular Biology Techniques
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                Medicine and Health Sciences
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                Custom metadata
                vor-update-to-uncorrected-proof
                2019-07-17
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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