Disentangling serology to elucidate henipa‐ and filovirus transmission in Madagascar fruit bats
Identifieur interne : 000721 ( Pmc/Checkpoint ); précédent : 000720; suivant : 000722Disentangling serology to elucidate henipa‐ and filovirus transmission in Madagascar fruit bats
Auteurs : Cara E. Brook ; Hafaliana C. Ranaivoson ; Christopher C. Broder ; Andrew A. Cunningham ; Jean-Michel Héraud ; Alison J. Peel ; Louise Gibson ; James L. N. Wood ; C. Jessica Metcalf ; Andrew P. DobsonSource :
- The Journal of Animal Ecology [ 0021-8790 ] ; 2019.
Abstract
Bats are reservoirs for emerging human pathogens, including Hendra and Nipah henipaviruses and Ebola and Marburg filoviruses. These viruses demonstrate predictable patterns in seasonality and age structure across multiple systems; previous work suggests that they may circulate in Madagascar's endemic fruit bats, which are widely consumed as human food. We aimed to (a) document the extent of henipa‐ and filovirus exposure among Malagasy fruit bats, (b) explore seasonality in seroprevalence and serostatus in these bat populations and (c) compare mechanistic hypotheses for possible transmission dynamics underlying these data. To this end, we amassed and analysed a unique dataset documenting longitudinal serological henipa‐ and filovirus dynamics in three Madagascar fruit bat species. We uncovered serological evidence of exposure to Hendra‐/Nipah‐related henipaviruses in Our findings suggest that bats may seasonally modulate mechanisms of pathogen control, with consequences for population‐level transmission. Additionally, we narrow the field of candidate transmission hypotheses by which bats are presumed to host and transmit potentially zoonotic viruses globally.
Url:
DOI: 10.1111/1365-2656.12985
PubMed: 30908623
PubMed Central: 7122791
Affiliations:
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Broder</name><affiliation><nlm:aff id="jane12985-aff-0004"></nlm:aff></affiliation></author><author><name sortKey="Cunningham, Andrew A" sort="Cunningham, Andrew A" uniqKey="Cunningham A" first="Andrew A." last="Cunningham">Andrew A. Cunningham</name><affiliation><nlm:aff id="jane12985-aff-0005"></nlm:aff></affiliation></author><author><name sortKey="Heraud, Jean Ichel" sort="Heraud, Jean Ichel" uniqKey="Heraud J" first="Jean-Michel" last="Héraud">Jean-Michel Héraud</name><affiliation><nlm:aff id="jane12985-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Peel, Alison J" sort="Peel, Alison J" uniqKey="Peel A" first="Alison J." last="Peel">Alison J. 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Brook</name><affiliation><nlm:aff id="jane12985-aff-0001"></nlm:aff></affiliation><affiliation><nlm:aff id="jane12985-curr-0001"></nlm:aff></affiliation></author><author><name sortKey="Ranaivoson, Hafaliana C" sort="Ranaivoson, Hafaliana C" uniqKey="Ranaivoson H" first="Hafaliana C." last="Ranaivoson">Hafaliana C. Ranaivoson</name><affiliation><nlm:aff id="jane12985-aff-0002"></nlm:aff></affiliation><affiliation><nlm:aff id="jane12985-aff-0003"></nlm:aff></affiliation></author><author><name sortKey="Broder, Christopher C" sort="Broder, Christopher C" uniqKey="Broder C" first="Christopher C." last="Broder">Christopher C. Broder</name><affiliation><nlm:aff id="jane12985-aff-0004"></nlm:aff></affiliation></author><author><name sortKey="Cunningham, Andrew A" sort="Cunningham, Andrew A" uniqKey="Cunningham A" first="Andrew A." last="Cunningham">Andrew A. Cunningham</name><affiliation><nlm:aff id="jane12985-aff-0005"></nlm:aff></affiliation></author><author><name sortKey="Heraud, Jean Ichel" sort="Heraud, Jean Ichel" uniqKey="Heraud J" first="Jean-Michel" last="Héraud">Jean-Michel Héraud</name><affiliation><nlm:aff id="jane12985-aff-0002"></nlm:aff></affiliation></author><author><name sortKey="Peel, Alison J" sort="Peel, Alison J" uniqKey="Peel A" first="Alison J." last="Peel">Alison J. Peel</name><affiliation><nlm:aff id="jane12985-aff-0006"></nlm:aff></affiliation></author><author><name sortKey="Gibson, Louise" sort="Gibson, Louise" uniqKey="Gibson L" first="Louise" last="Gibson">Louise Gibson</name><affiliation><nlm:aff id="jane12985-aff-0005"></nlm:aff></affiliation></author><author><name sortKey="Wood, James L N" sort="Wood, James L N" uniqKey="Wood J" first="James L. N." last="Wood">James L. N. Wood</name><affiliation><nlm:aff id="jane12985-aff-0007"></nlm:aff></affiliation></author><author><name sortKey="Metcalf, C Jessica" sort="Metcalf, C Jessica" uniqKey="Metcalf C" first="C. Jessica" last="Metcalf">C. Jessica Metcalf</name><affiliation><nlm:aff id="jane12985-aff-0001"></nlm:aff></affiliation></author><author><name sortKey="Dobson, Andrew P" sort="Dobson, Andrew P" uniqKey="Dobson A" first="Andrew P." last="Dobson">Andrew P. Dobson</name><affiliation><nlm:aff id="jane12985-aff-0001"></nlm:aff></affiliation></author></analytic><series><title level="j">The Journal of Animal Ecology</title><idno type="ISSN">0021-8790</idno><idno type="eISSN">1365-2656</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Abstract</title><p><list list-type="order" id="jane12985-list-0001"><list-item><p>Bats are reservoirs for emerging human pathogens, including Hendra and Nipah henipaviruses and Ebola and Marburg filoviruses. These viruses demonstrate predictable patterns in seasonality and age structure across multiple systems; previous work suggests that they may circulate in Madagascar's endemic fruit bats, which are widely consumed as human food.</p></list-item><list-item><p>We aimed to (a) document the extent of henipa‐ and filovirus exposure among Malagasy fruit bats, (b) explore seasonality in seroprevalence and serostatus in these bat populations and (c) compare mechanistic hypotheses for possible transmission dynamics underlying these data.</p></list-item><list-item><p>To this end, we amassed and analysed a unique dataset documenting longitudinal serological henipa‐ and filovirus dynamics in three Madagascar fruit bat species.</p></list-item><list-item><p>We uncovered serological evidence of exposure to Hendra‐/Nipah‐related henipaviruses in <italic>Eidolon dupreanum, Pteropus rufus</italic> and <italic>Rousettus madagascariensis,</italic> to Cedar‐related henipaviruses in <italic>E. dupreanum</italic> and <italic>R. madagascariensis</italic> and to Ebola‐related filoviruses in <italic>P. rufus</italic> and <italic>R. madagascariensis</italic>. We demonstrated significant seasonality in population‐level seroprevalence and individual serostatus for multiple viruses across these species, linked to the female reproductive calendar. An age‐structured subset of the data highlighted evidence of waning maternal antibodies in neonates, increasing seroprevalence in young and decreasing seroprevalence late in life. Comparison of mechanistic epidemiological models fit to these data offered support for transmission hypotheses permitting waning antibodies but retained immunity in adult‐age bats.</p></list-item><list-item><p>Our findings suggest that bats may seasonally modulate mechanisms of pathogen control, with consequences for population‐level transmission. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Anim Ecol</journal-id><journal-id journal-id-type="iso-abbrev">J Anim Ecol</journal-id><journal-id journal-id-type="doi">10.1111/(ISSN)1365-2656</journal-id><journal-id journal-id-type="publisher-id">JANE</journal-id><journal-title-group><journal-title>The Journal of Animal Ecology</journal-title></journal-title-group><issn pub-type="ppub">0021-8790</issn><issn pub-type="epub">1365-2656</issn><publisher><publisher-name>John Wiley and Sons Inc.</publisher-name><publisher-loc>Hoboken</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30908623</article-id><article-id pub-id-type="pmc">7122791</article-id><article-id pub-id-type="doi">10.1111/1365-2656.12985</article-id><article-id pub-id-type="publisher-id">JANE12985</article-id><article-categories><subj-group subj-group-type="overline"><subject>Research Article</subject></subj-group><subj-group subj-group-type="heading"><subject>Parasite and Disease Ecology</subject></subj-group></article-categories><title-group><article-title>Disentangling serology to elucidate henipa‐ and filovirus transmission in Madagascar fruit bats</article-title><alt-title alt-title-type="left-running-head">BROOK et al.</alt-title></title-group><contrib-group><contrib id="jane12985-cr-0001" contrib-type="author" corresp="yes"><name><surname>Brook</surname><given-names>Cara E.</given-names></name><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-4276-073X</contrib-id><xref ref-type="aff" rid="jane12985-aff-0001"><sup>1</sup></xref><xref ref-type="aff" rid="jane12985-curr-0001"><sup>8</sup></xref><address><email>cbrook@berkeley.edu</email></address></contrib><contrib id="jane12985-cr-0002" contrib-type="author"><name><surname>Ranaivoson</surname><given-names>Hafaliana C.</given-names></name><xref ref-type="aff" rid="jane12985-aff-0002"><sup>2</sup></xref><xref ref-type="aff" rid="jane12985-aff-0003"><sup>3</sup></xref></contrib><contrib id="jane12985-cr-0003" contrib-type="author"><name><surname>Broder</surname><given-names>Christopher C.</given-names></name><xref ref-type="aff" rid="jane12985-aff-0004"><sup>4</sup></xref></contrib><contrib id="jane12985-cr-0004" contrib-type="author"><name><surname>Cunningham</surname><given-names>Andrew A.</given-names></name><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-3543-6504</contrib-id><xref ref-type="aff" rid="jane12985-aff-0005"><sup>5</sup></xref></contrib><contrib id="jane12985-cr-0005" contrib-type="author"><name><surname>Héraud</surname><given-names>Jean‐Michel</given-names></name><xref ref-type="aff" rid="jane12985-aff-0002"><sup>2</sup></xref></contrib><contrib id="jane12985-cr-0006" contrib-type="author"><name><surname>Peel</surname><given-names>Alison J.</given-names></name><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-3538-3550</contrib-id><xref ref-type="aff" rid="jane12985-aff-0006"><sup>6</sup></xref></contrib><contrib id="jane12985-cr-0007" contrib-type="author"><name><surname>Gibson</surname><given-names>Louise</given-names></name><xref ref-type="aff" rid="jane12985-aff-0005"><sup>5</sup></xref></contrib><contrib id="jane12985-cr-0008" contrib-type="author"><name><surname>Wood</surname><given-names>James L. N.</given-names></name><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-0258-3188</contrib-id><xref ref-type="aff" rid="jane12985-aff-0007"><sup>7</sup></xref></contrib><contrib id="jane12985-cr-0009" contrib-type="author"><name><surname>Metcalf</surname><given-names>C. Jessica</given-names></name><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-3166-7521</contrib-id><xref ref-type="aff" rid="jane12985-aff-0001"><sup>1</sup></xref><xref ref-type="author-notes" rid="jane12985-note-1001"><sup>†</sup></xref></contrib><contrib id="jane12985-cr-0010" contrib-type="author"><name><surname>Dobson</surname><given-names>Andrew P.</given-names></name><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-9678-1694</contrib-id><xref ref-type="aff" rid="jane12985-aff-0001"><sup>1</sup></xref><xref ref-type="author-notes" rid="jane12985-note-1001"><sup>†</sup></xref></contrib></contrib-group><contrib-group><contrib id="jane12985-cr-0011" contrib-type="editor"><name><surname>Fenton</surname><given-names>Andy</given-names></name></contrib></contrib-group><aff id="jane12985-aff-0001"><label><sup>1</sup></label><named-content content-type="organisation-division">Department of Ecology & Evolutionary Biology</named-content><institution>Princeton University</institution><city>Princeton</city><named-content content-type="country-part">New Jersey</named-content></aff><aff id="jane12985-aff-0002"><label><sup>2</sup></label><named-content content-type="organisation-division">Virology Unit</named-content><institution>Institut Pasteur de Madagascar</institution><city>Antananarivo</city><country country="MG">Madagascar</country></aff><aff id="jane12985-aff-0003"><label><sup>3</sup></label><named-content content-type="organisation-division">Department of Animal Biology</named-content><institution>University of Antananarivo</institution><city>Antananarivo</city><country country="MG">Madagascar</country></aff><aff id="jane12985-aff-0004"><label><sup>4</sup></label><named-content content-type="organisation-division">Department of Microbiology and Immunology</named-content><institution>Uniformed Services University</institution><city>Bethesda</city><named-content content-type="country-part">Maryland</named-content></aff><aff id="jane12985-aff-0005"><label><sup>5</sup></label><named-content content-type="organisation-division">Institute of Zoology</named-content><institution>Zoological Society of London</institution><city>London</city><country country="GB">UK</country></aff><aff id="jane12985-aff-0006"><label><sup>6</sup></label><named-content content-type="organisation-division">Environmental Futures Research Institute</named-content><institution>Griffith University</institution><city>Nathan</city><named-content content-type="country-part">Queensland</named-content><country country="AU">Australia</country></aff><aff id="jane12985-aff-0007"><label><sup>7</sup></label><named-content content-type="organisation-division">Department of Veterinary Medicine</named-content><institution>University of Cambridge</institution><city>Cambridge</city><country country="GB">UK</country></aff><aff id="jane12985-curr-0001"><label><sup>8</sup></label>Present address:<named-content content-type="organisation-division">Department of Integrative Biology</named-content><institution>UC Berkeley</institution><city>Berkeley</city><named-content content-type="country-part">California.</named-content></aff><author-notes><corresp id="correspondenceTo"><label>*</label><bold>Correspondence</bold><break></break>Cara E. Brook<break></break>Email: <email>cbrook@berkeley.edu</email><break></break></corresp><fn fn-type="equal" id="jane12985-note-1001"><label>†</label><p>These senior authors contributed equally to this work.</p></fn></author-notes><pub-date pub-type="epub"><day>15</day><month>4</month><year>2019</year></pub-date><pub-date pub-type="ppub"><month>7</month><year>2019</year></pub-date><volume>88</volume><issue>7</issue><issue-id pub-id-type="doi">10.1111/jane.2019.88.issue-7</issue-id><fpage>1001</fpage><lpage>1016</lpage><history><date date-type="received"><day>30</day><month>8</month><year>2018</year></date><date date-type="accepted"><day>13</day><month>2</month><year>2019</year></date></history><permissions><pmc-comment> Journal of Animal Ecology © 2019 British Ecological Society </pmc-comment>
<copyright-statement content-type="article-copyright">© 2019 The Authors. Journal of Animal Ecology © 2019 British Ecological Society</copyright-statement><license><license-p>This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="file:JANE-88-1001.pdf"></self-uri><abstract id="jane12985-abs-0001"><title>Abstract</title><p><list list-type="order" id="jane12985-list-0001"><list-item><p>Bats are reservoirs for emerging human pathogens, including Hendra and Nipah henipaviruses and Ebola and Marburg filoviruses. These viruses demonstrate predictable patterns in seasonality and age structure across multiple systems; previous work suggests that they may circulate in Madagascar's endemic fruit bats, which are widely consumed as human food.</p></list-item><list-item><p>We aimed to (a) document the extent of henipa‐ and filovirus exposure among Malagasy fruit bats, (b) explore seasonality in seroprevalence and serostatus in these bat populations and (c) compare mechanistic hypotheses for possible transmission dynamics underlying these data.</p></list-item><list-item><p>To this end, we amassed and analysed a unique dataset documenting longitudinal serological henipa‐ and filovirus dynamics in three Madagascar fruit bat species.</p></list-item><list-item><p>We uncovered serological evidence of exposure to Hendra‐/Nipah‐related henipaviruses in <italic>Eidolon dupreanum, Pteropus rufus</italic> and <italic>Rousettus madagascariensis,</italic> to Cedar‐related henipaviruses in <italic>E. dupreanum</italic> and <italic>R. madagascariensis</italic> and to Ebola‐related filoviruses in <italic>P. rufus</italic> and <italic>R. madagascariensis</italic>. We demonstrated significant seasonality in population‐level seroprevalence and individual serostatus for multiple viruses across these species, linked to the female reproductive calendar. An age‐structured subset of the data highlighted evidence of waning maternal antibodies in neonates, increasing seroprevalence in young and decreasing seroprevalence late in life. Comparison of mechanistic epidemiological models fit to these data offered support for transmission hypotheses permitting waning antibodies but retained immunity in adult‐age bats.</p></list-item><list-item><p>Our findings suggest that bats may seasonally modulate mechanisms of pathogen control, with consequences for population‐level transmission. Additionally, we narrow the field of candidate transmission hypotheses by which bats are presumed to host and transmit potentially zoonotic viruses globally.</p></list-item></list></p></abstract><abstract abstract-type="graphical" id="jane12985-abs-0002"><p>In this paper, the authors (a) expand globally on the known range of bat hosts for henipaviruses and filoviruses, (b) demonstrate seasonal patterns in population‐level seroprevalence and individual‐level serostatus for Malagasy fruit bats and (c) use mechanistic models to reveal the critical role of waning humoral immunity in serological dynamics.<boxed-text position="anchor" content-type="graphic" id="jane12985-blkfxd-0001" orientation="portrait"><graphic xlink:href="JANE-88-1001-g005.jpg" position="anchor" id="nlm-graphic-1" orientation="portrait"></graphic></boxed-text></p></abstract><kwd-group kwd-group-type="author-generated"><kwd id="jane12985-kwd-0001">age–seroprevalence</kwd><kwd id="jane12985-kwd-0002">filovirus</kwd><kwd id="jane12985-kwd-0003">flying fox</kwd><kwd id="jane12985-kwd-0004">force of infection</kwd><kwd id="jane12985-kwd-0005">fruit bat</kwd><kwd id="jane12985-kwd-0006">henipavirus</kwd><kwd id="jane12985-kwd-0007">Madagascar</kwd><kwd id="jane12985-kwd-0008">zoonosis</kwd></kwd-group><funding-group><award-group id="funding-0001"><funding-source>Biological Defense Research Directorate (CCB)</funding-source></award-group><award-group id="funding-0002"><funding-source>AI054715 (CCB)</funding-source></award-group><award-group id="funding-0003"><funding-source>MR/P025226/1 (JLNW)</funding-source></award-group><award-group id="funding-0004"><funding-source>Veterinary Research Grant (JLNW)</funding-source></award-group><award-group id="funding-0005"><funding-source>Accelerate Postdoctoral Research Fellowship (AJP)</funding-source></award-group><award-group id="funding-0006"><funding-source>Center for Health and Well‐being Research Grant (CJEM)</funding-source></award-group><award-group id="funding-0007"><funding-source>Doctoral Dissertation Improvement (CEB)</funding-source><award-id>1600980</award-id></award-group><award-group id="funding-0008"><funding-source>Graduate Research Fellowship Program (CEB)</funding-source></award-group><award-group id="funding-0009"><funding-source>R01‐AI129822‐01 (JMH)</funding-source></award-group><award-group id="funding-0010"><funding-source>Young Explorer's Grant (CEB)</funding-source><award-id>YEG‐9269‐13</award-id></award-group><award-group id="funding-0011"><funding-source>Waitt Grant (CEB)</funding-source><award-id>W376‐15</award-id></award-group><award-group id="funding-0012"><funding-source>Walbridge Graduate Research Fund (CEB)</funding-source></award-group></funding-group><counts><fig-count count="4"></fig-count><table-count count="1"></table-count><page-count count="16"></page-count><word-count count="12417"></word-count></counts><custom-meta-group><custom-meta><meta-name>source-schema-version-number</meta-name><meta-value>2.0</meta-value></custom-meta><custom-meta><meta-name>cover-date</meta-name><meta-value>July 2019</meta-value></custom-meta><custom-meta><meta-name>details-of-publishers-convertor</meta-name><meta-value>Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.0 mode:remove_FC converted:15.04.2020</meta-value></custom-meta></custom-meta-group></article-meta><notes><p content-type="self-citation"><mixed-citation publication-type="journal" id="jane12985-cit-1001"><string-name><surname>Brook</surname><given-names>CE</given-names></string-name>, <string-name><surname>Ranaivoson</surname><given-names>HC</given-names></string-name>, <string-name><surname>Broder</surname><given-names>CC</given-names></string-name>, et al. <article-title>Disentangling serology to elucidate henipa‐ and filovirus transmission in Madagascar fruit bats</article-title>. <source xml:lang="en">J Anim Ecol</source>. <year>2019</year>;<volume>88</volume>:<fpage>1001</fpage>–<lpage>1016</lpage>. <pub-id pub-id-type="doi">10.1111/1365-2656.12985</pub-id><pub-id pub-id-type="pmid">30908623</pub-id></mixed-citation></p></notes></front></pmc><affiliations><list></list><tree><noCountry><name sortKey="Broder, Christopher C" sort="Broder, Christopher C" uniqKey="Broder C" first="Christopher C." last="Broder">Christopher C. Broder</name><name sortKey="Brook, Cara E" sort="Brook, Cara E" uniqKey="Brook C" first="Cara E." last="Brook">Cara E. Brook</name><name sortKey="Cunningham, Andrew A" sort="Cunningham, Andrew A" uniqKey="Cunningham A" first="Andrew A." last="Cunningham">Andrew A. Cunningham</name><name sortKey="Dobson, Andrew P" sort="Dobson, Andrew P" uniqKey="Dobson A" first="Andrew P." last="Dobson">Andrew P. Dobson</name><name sortKey="Gibson, Louise" sort="Gibson, Louise" uniqKey="Gibson L" first="Louise" last="Gibson">Louise Gibson</name><name sortKey="Heraud, Jean Ichel" sort="Heraud, Jean Ichel" uniqKey="Heraud J" first="Jean-Michel" last="Héraud">Jean-Michel Héraud</name><name sortKey="Metcalf, C Jessica" sort="Metcalf, C Jessica" uniqKey="Metcalf C" first="C. Jessica" last="Metcalf">C. Jessica Metcalf</name><name sortKey="Peel, Alison J" sort="Peel, Alison J" uniqKey="Peel A" first="Alison J." last="Peel">Alison J. Peel</name><name sortKey="Ranaivoson, Hafaliana C" sort="Ranaivoson, Hafaliana C" uniqKey="Ranaivoson H" first="Hafaliana C." last="Ranaivoson">Hafaliana C. Ranaivoson</name><name sortKey="Wood, James L N" sort="Wood, James L N" uniqKey="Wood J" first="James L. N." last="Wood">James L. N. Wood</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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