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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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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          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 references 33

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          Fever with thrombocytopenia associated with a novel bunyavirus in China.

          Heightened surveillance of acute febrile illness in China since 2009 has led to the identification of a severe fever with thrombocytopenia syndrome (SFTS) with an unknown cause. Infection with Anaplasma phagocytophilum has been suggested as a cause, but the pathogen has not been detected in most patients on laboratory testing. We obtained blood samples from patients with the case definition of SFTS in six provinces in China. The blood samples were used to isolate the causal pathogen by inoculation of cell culture and for detection of viral RNA on polymerase-chain-reaction assay. The pathogen was characterized on electron microscopy and nucleic acid sequencing. We used enzyme-linked immunosorbent assay, indirect immunofluorescence assay, and neutralization testing to analyze the level of virus-specific antibody in patients' serum samples. We isolated a novel virus, designated SFTS bunyavirus, from patients who presented with fever, thrombocytopenia, leukocytopenia, and multiorgan dysfunction. RNA sequence analysis revealed that the virus was a newly identified member of the genus phlebovirus in the Bunyaviridae family. Electron-microscopical examination revealed virions with the morphologic characteristics of a bunyavirus. The presence of the virus was confirmed in 171 patients with SFTS from six provinces by detection of viral RNA, specific antibodies to the virus in blood, or both. Serologic assays showed a virus-specific immune response in all 35 pairs of serum samples collected from patients during the acute and convalescent phases of the illness. A novel phlebovirus was identified in patients with a life-threatening illness associated with fever and thrombocytopenia in China. (Funded by the China Mega-Project for Infectious Diseases and others.).
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            The first identification and retrospective study of Severe Fever with Thrombocytopenia Syndrome in Japan.

            Severe fever with thrombocytopenia syndrome (SFTS) is caused by SFTS virus (SFTSV), a novel bunyavirus reported to be endemic in central and northeastern China. This article describes the first identified patient with SFTS and a retrospective study on SFTS in Japan.  Virologic and pathologic examinations were performed on the patient's samples. Laboratory diagnosis of SFTS was made by isolation/genome amplification and/or the detection of anti-SFTSV immunoglobulin G antibody in sera. Physicians were alerted to the initial diagnosis and asked whether they had previously treated patients with symptoms similar to those of SFTS. A female patient who died in 2012 received a diagnosis of SFTS. Ten additional patients with SFTS were then retrospectively identified. All patients were aged ≥50 years and lived in western Japan. Six cases were fatal. The ratio of males to females was 8:3. SFTSV was isolated from 8 patients. Phylogenetic analyses indicated that all of the Japanese SFTSV isolates formed a genotype independent to those from China. Most patients showed symptoms due to hemorrhage, possibly because of disseminated intravascular coagulation and/or hemophagocytosis. SFTS has been endemic to Japan, and SFTSV has been circulating naturally within the country.
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              Severe Fever with Thrombocytopenia Syndrome, South Korea, 2012

              We report a retrospectively identified fatal case of severe fever with thrombocytopenia syndrome (SFTS) in South Korea from 2012. SFTS virus was isolated from the stored blood of the patient. Phylogenetic analysis revealed this isolate was closely related to SFTS virus strains from China and Japan.
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                Author and article information

                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.

                Contributors
                Role: Funding acquisition, Role: Methodology, Role: Project administration, Role: Writing – original draft
                Role: Conceptualization, Role: Project administration
                Role: Formal analysis, Role: Funding acquisition
                Role: Resources, Role: Software
                Role: Software
                Role: Data curation, Role: Resources
                Role: Writing – review & editing
                Role: Conceptualization, Role: Funding acquisition, Role: Methodology, Role: Writing – original draft, Role: 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
                31276495 6636776 10.1371/journal.pntd.0006982 PNTD-D-18-01717
                © 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.

                Counts
                Figures: 4, Tables: 1, Pages: 14
                Product
                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
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                Social Sciences
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                Biology and Life Sciences
                Biochemistry
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                Medicine and Health Sciences
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                Ticks
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                Biology and Life Sciences
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                Invertebrates
                Arthropoda
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                Biology and Life Sciences
                Molecular Biology
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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

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