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      Human-animal interactions and bat coronavirus spillover potential among rural residents in Southern China

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          Abstract

          Human interaction with animals has been implicated as a primary risk factor for several high impact zoonoses, including many bat-origin viral diseases. However the animal-to-human spillover events that lead to emerging diseases are rarely observed or clinically examined, and the link between specific interactions and spillover risk is poorly understood. To investigate this phenomenon, we conducted biological-behavioral surveillance among rural residents in Yunnan, Guangxi, and Guangdong districts of Southern China, where we have identified a number of SARS-related coronaviruses in bats. Serum samples were tested for four bat-borne coronaviruses using newly developed enzyme-linked immunosorbent assays (ELISA). Survey data were used to characterize associations between human-animal contact and bat coronavirus spillover risk. A total of 1,596 residents were enrolled in the study from 2015 to 2017. Nine participants (0.6%) tested positive for bat coronaviruses. 265 (17%) participants reported severe acute respiratory infections (SARI) and/or influenza-like illness (ILI) symptoms in the past year, which were associated with poultry, carnivore, rodent/shrew, or bat contact, with variability by family income and district of residence. This study provides serological evidence of bat coronavirus spillover in rural communities in Southern China. The low seroprevalence observed in this study suggests that bat coronavirus spillover is a rare event. Nonetheless, this study highlights associations between human-animal interaction and zoonotic spillover risk. These findings can be used to support targeted biological behavioral surveillance in high-risk geographic areas in order to reduce the risk of zoonotic disease emergence.

          Highlights

          • Scientific question.

            • What are the behavioral risks in human-animal interactions that could lead to the emergence of bat coronaviruses in human population.

          • Evidence before this study.

            • Bat borne coronaviruses have caused several emerging infectious disease outbreaks of global significance, including SARS. Novel SARS-related coronaviruses have been discovered in bat populations in Southern China, some of which have the capacity to infect human cells. Human-animal interactions are thought to be critical for the emergence of bat coronaviruses, however the specific interactions linked to animal-to-human spillover remain unknown.

          • New Findings.

            • This study found serological evidence for bat-borne coronavirus transmission to people. Direct contact with bats was not identified as a risk factor. However, self-reported severe acute respiratory infection (SARI) and/or influenza-like illness (ILI) was linked to human interaction with other wildlife and livestock, suggesting that there may be other zoonotic exposures leading to clinical illness in these populations.

          • Significance of the study.

            • Findings from this study suggested that an integrated biological and behavioral surveillance in healthy community settings can help identify potential zoonotic disease spillover events or target surveillance to at-risk populations. This approach represents a potential early-warning system that could be used under non-outbreak conditions to identify potential zoonotic emerging diseases prior to largescale outbreaks.

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          Most cited references 27

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          Is Open Access

          Middle East Respiratory Syndrome Coronavirus in Bats, Saudi Arabia

          The source of human infection with Middle East respiratory syndrome coronavirus remains unknown. Molecular investigation indicated that bats in Saudi Arabia are infected with several alphacoronaviruses and betacoronaviruses. Virus from 1 bat showed 100% nucleotide identity to virus from the human index case-patient. Bats might play a role in human infection.
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            Discovery of swine as a host for the Reston ebolavirus.

            Since the discovery of the Marburg and Ebola species of filovirus, seemingly random, sporadic fatal outbreaks of disease in humans and nonhuman primates have given impetus to identification of host tropisms and potential reservoirs. Domestic swine in the Philippines, experiencing unusually severe outbreaks of porcine reproductive and respiratory disease syndrome, have now been discovered to host Reston ebolavirus (REBOV). Although REBOV is the only member of Filoviridae that has not been associated with disease in humans, its emergence in the human food chain is of concern. REBOV isolates were found to be more divergent from each other than from the original virus isolated in 1989, indicating polyphyletic origins and that REBOV has been circulating since, and possibly before, the initial discovery of REBOV in monkeys.
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              Synthetic recombinant bat SARS-like coronavirus is infectious in cultured cells and in mice.

              Defining prospective pathways by which zoonoses evolve and emerge as human pathogens is critical for anticipating and controlling both natural and deliberate pandemics. However, predicting tenable pathways of animal-to-human movement has been hindered by challenges in identifying reservoir species, cultivating zoonotic organisms in culture, and isolating full-length genomes for cloning and genetic studies. The ability to design and recover pathogens reconstituted from synthesized cDNAs has the potential to overcome these obstacles by allowing studies of replication and pathogenesis without identification of reservoir species or cultivation of primary isolates. Here, we report the design, synthesis, and recovery of the largest synthetic replicating life form, a 29.7-kb bat severe acute respiratory syndrome (SARS)-like coronavirus (Bat-SCoV), a likely progenitor to the SARS-CoV epidemic. To test a possible route of emergence from the noncultivable Bat-SCoV to human SARS-CoV, we designed a consensus Bat-SCoV genome and replaced the Bat-SCoV Spike receptor-binding domain (RBD) with the SARS-CoV RBD (Bat-SRBD). Bat-SRBD was infectious in cell culture and in mice and was efficiently neutralized by antibodies specific for both bat and human CoV Spike proteins. Rational design, synthesis, and recovery of hypothetical recombinant viruses can be used to investigate mechanisms of transspecies movement of zoonoses and has great potential to aid in rapid public health responses to known or predicted emerging microbial threats.
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                Author and article information

                Contributors
                Journal
                Biosafety and Health
                Chinese Medical Association Publishing House. Published by Elsevier B.V.
                2590-0536
                2590-0536
                9 November 2019
                September 2019
                9 November 2019
                : 1
                : 2
                : 84-90
                Affiliations
                [a ]EcoHealth Alliance, New York, NY, USA
                [b ]School of Education and Human Development, University of Colorado Denver, Denver, CO, USA
                [c ]Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China
                [d ]School of Health Sciences, Wuhan University, Wuhan 430071, China
                [e ]Directorate of Research, Business and Innovation, Kingston University, London, UK
                [f ]School of Life Science, Engineering and Computing, Kingston University, London, UK
                [g ]Mailman School of Public Health, Columbia University, New York, NY, USA
                Author notes
                []Corresponding author: CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China zlshi@ 123456wh.iov.cn
                [∗∗ ]Corresponding author: EcoHealth Alliance. 460 West 34th Street, New York, NY, 10001, USA daszak@ 123456ecohealthalliance.org
                Article
                S2590-0536(19)30030-8
                10.1016/j.bsheal.2019.10.004
                7148670
                © 2019 Chinese Medical Association Publishing House. Published by Elsevier B.V.

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

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