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

Identifieur interne : 003E74 ( Ncbi/Merge ); précédent : 003E73; suivant : 003E75

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

Auteurs : Hongying Li [États-Unis, Royaume-Uni] ; Emma Mendelsohn [États-Unis] ; Chen Zong [États-Unis] ; Wei Zhang [République populaire de Chine] ; Emily Hagan [États-Unis] ; Ning Wang [République populaire de Chine] ; Shiyue Li ; Hong Yan [République populaire de Chine] ; Huimin Huang [République populaire de Chine] ; Guangjian Zhu [États-Unis] ; Noam Ross [États-Unis] ; Aleksei Chmura [États-Unis] ; Philip Terry [Royaume-Uni] ; Mark Fielder [Royaume-Uni] ; Maureen Miller [États-Unis] ; Zhengli Shi [République populaire de Chine] ; Peter Daszak [États-Unis]

Source :

RBID : PMC:7148670

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.


Url:
DOI: 10.1016/j.bsheal.2019.10.004
PubMed: NONE
PubMed Central: 7148670

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PMC:7148670

Le document en format XML

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<name sortKey="Shi, Zhengli" sort="Shi, Zhengli" uniqKey="Shi Z" first="Zhengli" last="Shi">Zhengli Shi</name>
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<title xml:lang="en" level="a" type="main">Human-animal interactions and bat coronavirus spillover potential among rural residents in Southern China</title>
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<name sortKey="Zong, Chen" sort="Zong, Chen" uniqKey="Zong C" first="Chen" last="Zong">Chen Zong</name>
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<name sortKey="Hagan, Emily" sort="Hagan, Emily" uniqKey="Hagan E" first="Emily" last="Hagan">Emily Hagan</name>
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<name sortKey="Wang, Ning" sort="Wang, Ning" uniqKey="Wang N" first="Ning" last="Wang">Ning Wang</name>
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<name sortKey="Ross, Noam" sort="Ross, Noam" uniqKey="Ross N" first="Noam" last="Ross">Noam Ross</name>
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<name sortKey="Chmura, Aleksei" sort="Chmura, Aleksei" uniqKey="Chmura A" first="Aleksei" last="Chmura">Aleksei Chmura</name>
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<name sortKey="Terry, Philip" sort="Terry, Philip" uniqKey="Terry P" first="Philip" last="Terry">Philip Terry</name>
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<name sortKey="Fielder, Mark" sort="Fielder, Mark" uniqKey="Fielder M" first="Mark" last="Fielder">Mark Fielder</name>
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<nlm:aff id="aff6">School of Life Science, Engineering and Computing, Kingston University, London, UK</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>School of Life Science, Engineering and Computing, Kingston University, London</wicri:regionArea>
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<settlement type="city">Londres</settlement>
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</placeName>
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<name sortKey="Miller, Maureen" sort="Miller, Maureen" uniqKey="Miller M" first="Maureen" last="Miller">Maureen Miller</name>
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<region type="state">État de New York</region>
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</placeName>
<orgName type="university">Université Columbia</orgName>
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<author>
<name sortKey="Shi, Zhengli" sort="Shi, Zhengli" uniqKey="Shi Z" first="Zhengli" last="Shi">Zhengli Shi</name>
<affiliation wicri:level="1">
<nlm:aff id="aff3">Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071</wicri:regionArea>
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<settlement type="city">Wuhan</settlement>
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</author>
<author>
<name sortKey="Daszak, Peter" sort="Daszak, Peter" uniqKey="Daszak P" first="Peter" last="Daszak">Peter Daszak</name>
<affiliation wicri:level="2">
<nlm:aff id="aff1">EcoHealth Alliance, New York, NY, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>EcoHealth Alliance, New York, NY</wicri:regionArea>
<placeName>
<region type="state">État de New York</region>
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</affiliation>
</author>
</analytic>
<series>
<title level="j">Biosafety and Health</title>
<idno type="ISSN">2590-0536</idno>
<idno type="eISSN">2590-0536</idno>
<imprint>
<date when="2019">2019</date>
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</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass></textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<p>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.</p>
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<journal-title>Biosafety and Health</journal-title>
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<issn pub-type="ppub">2590-0536</issn>
<issn pub-type="epub">2590-0536</issn>
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<article-id pub-id-type="pmc">7148670</article-id>
<article-id pub-id-type="publisher-id">S2590-0536(19)30030-8</article-id>
<article-id pub-id-type="doi">10.1016/j.bsheal.2019.10.004</article-id>
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<contrib contrib-type="author" id="au9">
<name>
<surname>Huang</surname>
<given-names>Huimin</given-names>
</name>
<xref rid="aff4" ref-type="aff">d</xref>
</contrib>
<contrib contrib-type="author" id="au10">
<name>
<surname>Zhu</surname>
<given-names>Guangjian</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="au11">
<name>
<surname>Ross</surname>
<given-names>Noam</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="au12">
<name>
<surname>Chmura</surname>
<given-names>Aleksei</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author" id="au13">
<name>
<surname>Terry</surname>
<given-names>Philip</given-names>
</name>
<xref rid="aff5" ref-type="aff">e</xref>
</contrib>
<contrib contrib-type="author" id="au14">
<name>
<surname>Fielder</surname>
<given-names>Mark</given-names>
</name>
<xref rid="aff6" ref-type="aff">f</xref>
</contrib>
<contrib contrib-type="author" id="au15">
<name>
<surname>Miller</surname>
<given-names>Maureen</given-names>
</name>
<xref rid="aff7" ref-type="aff">g</xref>
</contrib>
<contrib contrib-type="author" id="au16">
<name>
<surname>Shi</surname>
<given-names>Zhengli</given-names>
</name>
<email>zlshi@wh.iov.cn</email>
<xref rid="aff3" ref-type="aff">c</xref>
<xref rid="cor1" ref-type="corresp"></xref>
</contrib>
<contrib contrib-type="author" id="au17">
<name>
<surname>Daszak</surname>
<given-names>Peter</given-names>
</name>
<email>daszak@ecohealthalliance.org</email>
<xref rid="aff1" ref-type="aff">a</xref>
<xref rid="cor2" ref-type="corresp">∗∗</xref>
</contrib>
</contrib-group>
<aff id="aff1">
<label>a</label>
EcoHealth Alliance, New York, NY, USA</aff>
<aff id="aff2">
<label>b</label>
School of Education and Human Development, University of Colorado Denver, Denver, CO, USA</aff>
<aff id="aff3">
<label>c</label>
Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China</aff>
<aff id="aff4">
<label>d</label>
School of Health Sciences, Wuhan University, Wuhan 430071, China</aff>
<aff id="aff5">
<label>e</label>
Directorate of Research, Business and Innovation, Kingston University, London, UK</aff>
<aff id="aff6">
<label>f</label>
School of Life Science, Engineering and Computing, Kingston University, London, UK</aff>
<aff id="aff7">
<label>g</label>
Mailman School of Public Health, Columbia University, New York, NY, USA</aff>
<author-notes>
<corresp id="cor1">
<label></label>
Corresponding author: CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China
<email>zlshi@wh.iov.cn</email>
</corresp>
<corresp id="cor2">
<label>∗∗</label>
Corresponding author: EcoHealth Alliance. 460 West 34th Street, New York, NY, 10001, USA
<email>daszak@ecohealthalliance.org</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release">
<day>9</day>
<month>11</month>
<year>2019</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub">
<month>9</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub">
<day>9</day>
<month>11</month>
<year>2019</year>
</pub-date>
<volume>1</volume>
<issue>2</issue>
<fpage>84</fpage>
<lpage>90</lpage>
<history>
<date date-type="received">
<day>9</day>
<month>7</month>
<year>2019</year>
</date>
<date date-type="rev-recd">
<day>26</day>
<month>10</month>
<year>2019</year>
</date>
<date date-type="accepted">
<day>28</day>
<month>10</month>
<year>2019</year>
</date>
</history>
<permissions>
<copyright-statement>© 2019 Chinese Medical Association Publishing House. Published by Elsevier B.V.</copyright-statement>
<copyright-year>2019</copyright-year>
<copyright-holder>Elsevier B.V.</copyright-holder>
<license>
<license-p>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.</license-p>
</license>
</permissions>
<abstract id="abs0010">
<p>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.</p>
</abstract>
<abstract abstract-type="author-highlights" id="abs0015">
<title>Highlights</title>
<p>
<list list-type="simple" id="olist0010">
<list-item id="u0010">
<p id="p0010">Scientific question.
<list list-type="simple" id="olist0015">
<list-item id="o0010">
<label></label>
<p id="p0015">What are the behavioral risks in human-animal interactions that could lead to the emergence of bat coronaviruses in human population.</p>
</list-item>
</list>
</p>
</list-item>
<list-item id="u0015">
<p id="p0020">Evidence before this study.
<list list-type="simple" id="ulist0010">
<list-item id="u0020">
<label></label>
<p id="p0025">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.</p>
</list-item>
</list>
</p>
</list-item>
<list-item id="u0025">
<p id="p0030">New Findings.
<list list-type="simple" id="ulist0015">
<list-item id="u0030">
<label></label>
<p id="p0035">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.</p>
</list-item>
</list>
</p>
</list-item>
<list-item id="u0035">
<p id="p0040">Significance of the study.
<list list-type="simple" id="ulist0020">
<list-item id="u0040">
<label></label>
<p id="p0045">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.</p>
</list-item>
</list>
</p>
</list-item>
</list>
</p>
</abstract>
<kwd-group id="kwrds0010">
<title>Keywords</title>
<kwd>Bat coronavirus</kwd>
<kwd>Human-animal interaction</kwd>
<kwd>Disease emergence</kwd>
<kwd>Southern China</kwd>
<kwd>Rural community</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>Royaume-Uni</li>
<li>République populaire de Chine</li>
<li>États-Unis</li>
</country>
<region>
<li>Angleterre</li>
<li>Colorado</li>
<li>Grand Londres</li>
<li>Hubei</li>
<li>État de New York</li>
</region>
<settlement>
<li>Londres</li>
<li>New York</li>
<li>Wuhan</li>
</settlement>
<orgName>
<li>Université Columbia</li>
<li>Université de Wuhan</li>
</orgName>
</list>
<tree>
<noCountry>
<name sortKey="Li, Shiyue" sort="Li, Shiyue" uniqKey="Li S" first="Shiyue" last="Li">Shiyue Li</name>
</noCountry>
<country name="États-Unis">
<region name="État de New York">
<name sortKey="Li, Hongying" sort="Li, Hongying" uniqKey="Li H" first="Hongying" last="Li">Hongying Li</name>
</region>
<name sortKey="Chmura, Aleksei" sort="Chmura, Aleksei" uniqKey="Chmura A" first="Aleksei" last="Chmura">Aleksei Chmura</name>
<name sortKey="Daszak, Peter" sort="Daszak, Peter" uniqKey="Daszak P" first="Peter" last="Daszak">Peter Daszak</name>
<name sortKey="Hagan, Emily" sort="Hagan, Emily" uniqKey="Hagan E" first="Emily" last="Hagan">Emily Hagan</name>
<name sortKey="Mendelsohn, Emma" sort="Mendelsohn, Emma" uniqKey="Mendelsohn E" first="Emma" last="Mendelsohn">Emma Mendelsohn</name>
<name sortKey="Miller, Maureen" sort="Miller, Maureen" uniqKey="Miller M" first="Maureen" last="Miller">Maureen Miller</name>
<name sortKey="Ross, Noam" sort="Ross, Noam" uniqKey="Ross N" first="Noam" last="Ross">Noam Ross</name>
<name sortKey="Zhu, Guangjian" sort="Zhu, Guangjian" uniqKey="Zhu G" first="Guangjian" last="Zhu">Guangjian Zhu</name>
<name sortKey="Zong, Chen" sort="Zong, Chen" uniqKey="Zong C" first="Chen" last="Zong">Chen Zong</name>
</country>
<country name="Royaume-Uni">
<region name="Angleterre">
<name sortKey="Li, Hongying" sort="Li, Hongying" uniqKey="Li H" first="Hongying" last="Li">Hongying Li</name>
</region>
<name sortKey="Fielder, Mark" sort="Fielder, Mark" uniqKey="Fielder M" first="Mark" last="Fielder">Mark Fielder</name>
<name sortKey="Terry, Philip" sort="Terry, Philip" uniqKey="Terry P" first="Philip" last="Terry">Philip Terry</name>
</country>
<country name="République populaire de Chine">
<region name="Hubei">
<name sortKey="Zhang, Wei" sort="Zhang, Wei" uniqKey="Zhang W" first="Wei" last="Zhang">Wei Zhang</name>
</region>
<name sortKey="Huang, Huimin" sort="Huang, Huimin" uniqKey="Huang H" first="Huimin" last="Huang">Huimin Huang</name>
<name sortKey="Shi, Zhengli" sort="Shi, Zhengli" uniqKey="Shi Z" first="Zhengli" last="Shi">Zhengli Shi</name>
<name sortKey="Wang, Ning" sort="Wang, Ning" uniqKey="Wang N" first="Ning" last="Wang">Ning Wang</name>
<name sortKey="Yan, Hong" sort="Yan, Hong" uniqKey="Yan H" first="Hong" last="Yan">Hong Yan</name>
</country>
</tree>
</affiliations>
</record>

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