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Incidence of influenza A(H3N2) virus infections in Hong Kong in a longitudinal sero-epidemiological study, 2009-2015

Identifieur interne : 000C60 ( Pmc/Curation ); précédent : 000C59; suivant : 000C61

Incidence of influenza A(H3N2) virus infections in Hong Kong in a longitudinal sero-epidemiological study, 2009-2015

Auteurs : Vivian W. I. Wei [République populaire de Chine] ; Jessica Y. T. Wong [République populaire de Chine] ; Ranawaka A. P. M. Perera [République populaire de Chine] ; Kin On Kwok [République populaire de Chine] ; Vicky J. Fang [République populaire de Chine] ; Ian G. Barr [Australie] ; J. S. Malik Peiris [République populaire de Chine] ; Steven Riley [Royaume-Uni] ; Benjamin J. Cowling [République populaire de Chine]

Source :

RBID : PMC:5967746

Abstract

Background

Many serologic studies were done during and after the 2009 influenza pandemic, to estimate the cumulative incidence of influenza A(H1N1)pdm09 virus infections, but there are few comparative estimates of the incidence of influenza A(H3N2) virus infections during epidemics.

Methods

We conducted a longitudinal serologic study in Hong Kong. We collected sera annually and tested samples from 2009–13 by HAI against the A/Perth/16/2009(H3N2) virus, and samples from 2013–15 against the A/Victoria/361/2011(H3N2) virus using the hemagglutination inhibition (HAI) assay. We estimated the cumulative incidence of infections based on 4-fold or greater rises in HAI titers in consecutive sera.

Results

There were four major H3N2 epidemics: (1) Aug-Oct 2010; (2) Mar-Jun 2012; (3) Jul-Oct 2013; and (4) Jun-Jul 2014. Between 516 and 619 relevant pairs of sera were available for each epidemic. We estimated that 9%, 19%, 7% and 7% of the population were infected in each epidemic, respectively, with higher incidence in children in epidemics 1 and 4.

Conclusions

We found that re-infections in each of the four H3N2 epidemics that occurred from 2010 through 2014 were rare. The largest H3N2 epidemic occurred with the lowest level of pre-epidemic immunity.


Url:
DOI: 10.1371/journal.pone.0197504
PubMed: 29795587
PubMed Central: 5967746

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PMC:5967746

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<name sortKey="Perera, Ranawaka A P M" sort="Perera, Ranawaka A P M" uniqKey="Perera R" first="Ranawaka A. P. M." last="Perera">Ranawaka A. P. M. Perera</name>
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</nlm:aff>
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<wicri:regionArea>Shenzhen Research Institute of the Chinese University of Hong Kong, Shenzhen</wicri:regionArea>
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<name sortKey="Fang, Vicky J" sort="Fang, Vicky J" uniqKey="Fang V" first="Vicky J." last="Fang">Vicky J. Fang</name>
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<name sortKey="Barr, Ian G" sort="Barr, Ian G" uniqKey="Barr I" first="Ian G." last="Barr">Ian G. Barr</name>
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<wicri:regionArea>WHO Collaborating Centre for Reference and Research, Melbourne, Victoria</wicri:regionArea>
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<addr-line>Department of Microbiology and Immunology, University of Melbourne, Melbourne, Victoria, Australia</addr-line>
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<name sortKey="Peiris, J S Malik" sort="Peiris, J S Malik" uniqKey="Peiris J" first="J. S. Malik" last="Peiris">J. S. Malik Peiris</name>
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<name sortKey="Riley, Steven" sort="Riley, Steven" uniqKey="Riley S" first="Steven" last="Riley">Steven Riley</name>
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<wicri:regionArea>MRC Centre for Outbreak Analysis and Modelling, Department for Infectious Disease Epidemiology, Imperial College London, London</wicri:regionArea>
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<sec id="sec001">
<title>Background</title>
<p>Many serologic studies were done during and after the 2009 influenza pandemic, to estimate the cumulative incidence of influenza A(H1N1)pdm09 virus infections, but there are few comparative estimates of the incidence of influenza A(H3N2) virus infections during epidemics.</p>
</sec>
<sec id="sec002">
<title>Methods</title>
<p>We conducted a longitudinal serologic study in Hong Kong. We collected sera annually and tested samples from 2009–13 by HAI against the A/Perth/16/2009(H3N2) virus, and samples from 2013–15 against the A/Victoria/361/2011(H3N2) virus using the hemagglutination inhibition (HAI) assay. We estimated the cumulative incidence of infections based on 4-fold or greater rises in HAI titers in consecutive sera.</p>
</sec>
<sec id="sec003">
<title>Results</title>
<p>There were four major H3N2 epidemics: (1) Aug-Oct 2010; (2) Mar-Jun 2012; (3) Jul-Oct 2013; and (4) Jun-Jul 2014. Between 516 and 619 relevant pairs of sera were available for each epidemic. We estimated that 9%, 19%, 7% and 7% of the population were infected in each epidemic, respectively, with higher incidence in children in epidemics 1 and 4.</p>
</sec>
<sec id="sec004">
<title>Conclusions</title>
<p>We found that re-infections in each of the four H3N2 epidemics that occurred from 2010 through 2014 were rare. The largest H3N2 epidemic occurred with the lowest level of pre-epidemic immunity.</p>
</sec>
</div>
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<alt-title alt-title-type="running-head">Serologic study of influenza A(H3N2)</alt-title>
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<contrib-group>
<contrib contrib-type="author" equal-contrib="yes">
<name>
<surname>Wei</surname>
<given-names>Vivian W. I.</given-names>
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<role content-type="http://credit.casrai.org/">Data curation</role>
<role content-type="http://credit.casrai.org/">Formal analysis</role>
<role content-type="http://credit.casrai.org/">Project administration</role>
<role content-type="http://credit.casrai.org/">Writing – original draft</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes">
<name>
<surname>Wong</surname>
<given-names>Jessica Y. T.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Formal analysis</role>
<role content-type="http://credit.casrai.org/">Writing – original draft</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Perera</surname>
<given-names>Ranawaka A. P. M.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Methodology</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff003">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kwok</surname>
<given-names>Kin On</given-names>
</name>
<role content-type="http://credit.casrai.org/">Project administration</role>
<role content-type="http://credit.casrai.org/">Supervision</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff002">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff004">
<sup>4</sup>
</xref>
<xref ref-type="aff" rid="aff005">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Fang</surname>
<given-names>Vicky J.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Data curation</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Barr</surname>
<given-names>Ian G.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Resources</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff006">
<sup>6</sup>
</xref>
<xref ref-type="aff" rid="aff007">
<sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Peiris</surname>
<given-names>J. S. Malik</given-names>
</name>
<role content-type="http://credit.casrai.org/">Methodology</role>
<role content-type="http://credit.casrai.org/">Resources</role>
<role content-type="http://credit.casrai.org/">Supervision</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff003">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Riley</surname>
<given-names>Steven</given-names>
</name>
<role content-type="http://credit.casrai.org/">Conceptualization</role>
<role content-type="http://credit.casrai.org/">Funding acquisition</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff008">
<sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-6297-7154</contrib-id>
<name>
<surname>Cowling</surname>
<given-names>Benjamin J.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Conceptualization</role>
<role content-type="http://credit.casrai.org/">Funding acquisition</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor001">*</xref>
</contrib>
</contrib-group>
<aff id="aff001">
<label>1</label>
<addr-line>WHO Collaborating Centre for Infectious Disease Epidemiology and Control, School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, Hong Kong Special Administrative Region, China</addr-line>
</aff>
<aff id="aff002">
<label>2</label>
<addr-line>Jockey Club School of Public Health and Primary Care, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong Special Administrative Region, China</addr-line>
</aff>
<aff id="aff003">
<label>3</label>
<addr-line>Centre of Influenza Research, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, Hong Kong Special Administrative Region, China</addr-line>
</aff>
<aff id="aff004">
<label>4</label>
<addr-line>Stanley Ho Centre for Emerging Infectious Diseases, The Chinese University of Hong Kong, Shatin, Hong Kong, Hong Kong Special Administrative Region, China</addr-line>
</aff>
<aff id="aff005">
<label>5</label>
<addr-line>Shenzhen Research Institute of the Chinese University of Hong Kong, Shenzhen, China</addr-line>
</aff>
<aff id="aff006">
<label>6</label>
<addr-line>WHO Collaborating Centre for Reference and Research, Melbourne, Victoria, Australia</addr-line>
</aff>
<aff id="aff007">
<label>7</label>
<addr-line>Department of Microbiology and Immunology, University of Melbourne, Melbourne, Victoria, Australia</addr-line>
</aff>
<aff id="aff008">
<label>8</label>
<addr-line>MRC Centre for Outbreak Analysis and Modelling, Department for Infectious Disease Epidemiology, Imperial College London, London, United Kingdom</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Nishiura</surname>
<given-names>Hiroshi</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>Hokkaido University Graduate School of Medicine, JAPAN</addr-line>
</aff>
<author-notes>
<fn fn-type="COI-statement" id="coi001">
<p>
<bold>Competing Interests: </bold>
I have read the journal's policy and the authors of this manuscript have the following competing interests: BJC has received research funding from Sanofi Pasteur for a study of influenza vaccine effectiveness. BJC is a Section Editor of PLoS ONE. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials. The authors report no other potential conflicts of interest.</p>
</fn>
<corresp id="cor001">* E-mail:
<email>bcowling@hku.hk</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>24</day>
<month>5</month>
<year>2018</year>
</pub-date>
<pub-date pub-type="collection">
<year>2018</year>
</pub-date>
<volume>13</volume>
<issue>5</issue>
<elocation-id>e0197504</elocation-id>
<history>
<date date-type="received">
<day>30</day>
<month>11</month>
<year>2017</year>
</date>
<date date-type="accepted">
<day>3</day>
<month>5</month>
<year>2018</year>
</date>
</history>
<permissions>
<copyright-statement>© 2018 Wei et al</copyright-statement>
<copyright-year>2018</copyright-year>
<copyright-holder>Wei et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<license-p>This is an open access article distributed under the terms of the
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="pone.0197504.pdf"></self-uri>
<abstract>
<sec id="sec001">
<title>Background</title>
<p>Many serologic studies were done during and after the 2009 influenza pandemic, to estimate the cumulative incidence of influenza A(H1N1)pdm09 virus infections, but there are few comparative estimates of the incidence of influenza A(H3N2) virus infections during epidemics.</p>
</sec>
<sec id="sec002">
<title>Methods</title>
<p>We conducted a longitudinal serologic study in Hong Kong. We collected sera annually and tested samples from 2009–13 by HAI against the A/Perth/16/2009(H3N2) virus, and samples from 2013–15 against the A/Victoria/361/2011(H3N2) virus using the hemagglutination inhibition (HAI) assay. We estimated the cumulative incidence of infections based on 4-fold or greater rises in HAI titers in consecutive sera.</p>
</sec>
<sec id="sec003">
<title>Results</title>
<p>There were four major H3N2 epidemics: (1) Aug-Oct 2010; (2) Mar-Jun 2012; (3) Jul-Oct 2013; and (4) Jun-Jul 2014. Between 516 and 619 relevant pairs of sera were available for each epidemic. We estimated that 9%, 19%, 7% and 7% of the population were infected in each epidemic, respectively, with higher incidence in children in epidemics 1 and 4.</p>
</sec>
<sec id="sec004">
<title>Conclusions</title>
<p>We found that re-infections in each of the four H3N2 epidemics that occurred from 2010 through 2014 were rare. The largest H3N2 epidemic occurred with the lowest level of pre-epidemic immunity.</p>
</sec>
</abstract>
<funding-group>
<award-group id="award001">
<funding-source>
<institution-wrap>
<institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100005847</institution-id>
<institution>Health and Medical Research Fund</institution>
</institution-wrap>
</funding-source>
<award-id>13120732</award-id>
<principal-award-recipient>
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-6297-7154</contrib-id>
<name>
<surname>Cowling</surname>
<given-names>Benjamin J.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award002">
<funding-source>
<institution>Research Fund for the Control of Infectious Diseases</institution>
</funding-source>
<award-id>PHE-21</award-id>
<principal-award-recipient>
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-6297-7154</contrib-id>
<name>
<surname>Cowling</surname>
<given-names>Benjamin J.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award003">
<funding-source>
<institution>Area of Excellence Scheme of the University Grants Committee of Hong Kong</institution>
</funding-source>
<award-id>AoE/M-12/06</award-id>
<principal-award-recipient>
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-6297-7154</contrib-id>
<name>
<surname>Cowling</surname>
<given-names>Benjamin J.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award004">
<funding-source>
<institution>Medical Research Council</institution>
</funding-source>
<award-id>Project MR/J008761/1</award-id>
<principal-award-recipient>
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-6297-7154</contrib-id>
<name>
<surname>Cowling</surname>
<given-names>Benjamin J.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award005">
<funding-source>
<institution-wrap>
<institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100004440</institution-id>
<institution>Wellcome Trust</institution>
</institution-wrap>
</funding-source>
<award-id>Project 093488/Z/10/Z Investigator Award 200861/Z/16/Z</award-id>
<principal-award-recipient>
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-6297-7154</contrib-id>
<name>
<surname>Cowling</surname>
<given-names>Benjamin J.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award006">
<funding-source>
<institution>National Institute for General Medical Sciences</institution>
</funding-source>
<award-id>MIDAS U01 GM110721-01</award-id>
<principal-award-recipient>
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-6297-7154</contrib-id>
<name>
<surname>Cowling</surname>
<given-names>Benjamin J.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award007">
<funding-source>
<institution-wrap>
<institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100000272</institution-id>
<institution>National Institute for Health Research</institution>
</institution-wrap>
</funding-source>
<award-id>Health Protection Research Unit funding</award-id>
<principal-award-recipient>
<contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-6297-7154</contrib-id>
<name>
<surname>Cowling</surname>
<given-names>Benjamin J.</given-names>
</name>
</principal-award-recipient>
</award-group>
<funding-statement>This project was supported by the Health and Medical Research Fund, Hong Kong (grant no. 13120732), the Research Grants Council, Hong Kong (grant no. 776810), the Research Fund for the Control of Infectious Diseases, Hong Kong (grant no: PHE-21), the Area of Excellence Scheme of the University Grants Committee of Hong Kong (grant no. AoE/M-12/06), and the Research Grants Council of the Hong Kong Special Administrative Region, China (project No. T11-705/14N). SR acknowledges support from Wellcome Trust (200861/Z/16/Z); Medical Research Council, UK (Project MR/J008761/1); National Institute for Health Research (UK, for Health Protection Research Unit funding); the National Institute of General Medical Sciences (MIDAS U01 GM110721-01). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts>
<fig-count count="4"></fig-count>
<table-count count="2"></table-count>
<page-count count="11"></page-count>
</counts>
<custom-meta-group>
<custom-meta id="data-availability">
<meta-name>Data Availability</meta-name>
<meta-value>Raw data are available via Dryad at: doi:
<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.5061/dryad.7c93n5s">10.5061/dryad.7c93n5s</ext-link>
.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes>
<title>Data Availability</title>
<p>Raw data are available via Dryad at: doi:
<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.5061/dryad.7c93n5s">10.5061/dryad.7c93n5s</ext-link>
.</p>
</notes>
</front>
</pmc>
</record>

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