Genesis and pathogenesis of the 1918 pandemic H1N1 influenza A virus
Identifieur interne : 000A42 ( Ncbi/Merge ); précédent : 000A41; suivant : 000A43Genesis and pathogenesis of the 1918 pandemic H1N1 influenza A virus
Auteurs : Michael Worobey ; Guan-Zhu Han ; Andrew Rambaut [Royaume-Uni]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2014.
Abstract
The origin of the 1918 pandemic influenza A virus (IAV) and the reasons for its unusual severity are two of the foremost biomedical mysteries of the past century. We infer that the virus arose via reassortment between a preexisting human H1 IAV lineage and an avian virus. Phylogenetic, seroarcheological, and epidemiological evidence indicates those born earlier or later than ∼1880–1900 would have had some protection against the 1918 H1N1 virus, whereas many young adults born from ∼1880–1900 may have lacked such protection because of childhood exposure to an antigenically distinct H3N8 virus. Our findings suggest that better understanding of how initial exposure shapes lifetime immunity may enhance the prediction and control of future IAV pandemics and seasonal epidemics.
Url:
DOI: 10.1073/pnas.1324197111
PubMed: 24778238
PubMed Central: 4050607
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<author><name sortKey="Han, Guan Zhu" sort="Han, Guan Zhu" uniqKey="Han G" first="Guan-Zhu" last="Han">Guan-Zhu Han</name>
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85721;</nlm:aff>
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<author><name sortKey="Han, Guan Zhu" sort="Han, Guan Zhu" uniqKey="Han G" first="Guan-Zhu" last="Han">Guan-Zhu Han</name>
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85721;</nlm:aff>
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20892</nlm:aff>
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<series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
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<front><div type="abstract" xml:lang="en"><title>Significance</title>
<p>The origin of the 1918 pandemic influenza A virus (IAV) and the reasons for its unusual severity are two of the foremost biomedical mysteries of the past century. We infer that the virus arose via reassortment between a preexisting human H1 IAV lineage and an avian virus. Phylogenetic, seroarcheological, and epidemiological evidence indicates those born earlier or later than ∼1880–1900 would have had some protection against the 1918 H1N1 virus, whereas many young adults born from ∼1880–1900 may have lacked such protection because of childhood exposure to an antigenically distinct H3N8 virus. Our findings suggest that better understanding of how initial exposure shapes lifetime immunity may enhance the prediction and control of future IAV pandemics and seasonal epidemics.</p>
</div>
</front>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
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<article-id pub-id-type="pmc">4050607</article-id>
<article-id pub-id-type="publisher-id">201324197</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1324197111</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Evolution</subject>
</subj-group>
</subj-group>
<series-title>From the Cover</series-title>
</article-categories>
<title-group><article-title>Genesis and pathogenesis of the 1918 pandemic H1N1 influenza A virus</article-title>
<alt-title alt-title-type="short">Origins and pathogenesis of the 1918 flu pandemic</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Worobey</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>1</sup>
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<contrib contrib-type="author"><name><surname>Han</surname>
<given-names>Guan-Zhu</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rambaut</surname>
<given-names>Andrew</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>d</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
Department of Ecology and Evolutionary Biology,<institution>University of Arizona</institution>
, Tucson,<addr-line>AZ</addr-line>
85721;</aff>
<aff id="aff2"><sup>b</sup>
Institute of Evolutionary Biology and</aff>
<aff id="aff4"><sup>c</sup>
Centre for Infection, Immunity, and Evolution,<institution>University of Edinburgh</institution>
, Edinburgh EH9 3JT,<country>United Kingdom</country>
; and</aff>
<aff id="aff3"><sup>d</sup>
Fogarty International Center,<institution>National Institutes of Health</institution>
, Bethesda,<addr-line>MD</addr-line>
20892</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>1</sup>
To whom correspondence should be addressed. E-mail: <email>worobey@email.arizona.edu</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Neil M. Ferguson, Imperial College London, London, United Kingdom, and accepted by the Editorial Board April 8, 2014 (received for review December 30, 2013)</p>
</fn>
<fn fn-type="con"><p>Author contributions: M.W. designed research; M.W., G.-Z.H., and A.R. performed research; M.W., G.-Z.H., and A.R. analyzed data; and M.W. devised the age-specific mortality model and wrote the paper.</p>
</fn>
<fn fn-type="conflict"><p>The authors declare no conflict of interest.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>3</day>
<month>6</month>
<year>2014</year>
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<pub-date pub-type="epub"><day>28</day>
<month>4</month>
<year>2014</year>
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<month>4</month>
<year>2014</year>
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<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
. </pmc-comment>
<volume>111</volume>
<issue>22</issue>
<fpage>8107</fpage>
<lpage>8112</lpage>
<permissions><license license-type="open-access"><license-p>Freely available online through the PNAS open access option.</license-p>
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</permissions>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201324197.pdf"></self-uri>
<abstract abstract-type="executive-summary"><title>Significance</title>
<p>The origin of the 1918 pandemic influenza A virus (IAV) and the reasons for its unusual severity are two of the foremost biomedical mysteries of the past century. We infer that the virus arose via reassortment between a preexisting human H1 IAV lineage and an avian virus. Phylogenetic, seroarcheological, and epidemiological evidence indicates those born earlier or later than ∼1880–1900 would have had some protection against the 1918 H1N1 virus, whereas many young adults born from ∼1880–1900 may have lacked such protection because of childhood exposure to an antigenically distinct H3N8 virus. Our findings suggest that better understanding of how initial exposure shapes lifetime immunity may enhance the prediction and control of future IAV pandemics and seasonal epidemics.</p>
</abstract>
<abstract><p>The source, timing, and geographical origin of the 1918–1920 pandemic influenza A virus have remained tenaciously obscure for nearly a century, as have the reasons for its unusual severity among young adults. Here, we reconstruct the origins of the pandemic virus and the classic swine influenza and (postpandemic) seasonal H1N1 lineages using a host-specific molecular clock approach that is demonstrably more accurate than previous methods. Our results suggest that the 1918 pandemic virus originated shortly before 1918 when a human H1 virus, which we infer emerged before ∼1907, acquired avian N1 neuraminidase and internal protein genes. We find that the resulting pandemic virus jumped directly to swine but was likely displaced in humans by ∼1922 by a reassortant with an antigenically distinct H1 HA. Hence, although the swine lineage was a direct descendent of the pandemic virus, the post-1918 seasonal H1N1 lineage evidently was not, at least for HA. These findings help resolve several seemingly disparate observations from 20th century influenza epidemiology, seroarcheology, and immunology. The phylogenetic results, combined with these other lines of evidence, suggest that the high mortality in 1918 among adults aged ∼20 to ∼40 y may have been due primarily to their childhood exposure to a doubly heterosubtypic putative H3N8 virus, which we estimate circulated from ∼1889–1900. All other age groups (except immunologically naive infants) were likely partially protected by childhood exposure to N1 and/or H1-related antigens. Similar processes may underlie age-specific mortality differences between seasonal H1N1 vs. H3N2 and human H5N1 vs. H7N9 infections.</p>
</abstract>
<kwd-group><kwd>phylogeny</kwd>
<kwd>cohort immunity</kwd>
<kwd>pathogenicity</kwd>
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<affiliations><list><country><li>Royaume-Uni</li>
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<country name="Royaume-Uni"><noRegion><name sortKey="Rambaut, Andrew" sort="Rambaut, Andrew" uniqKey="Rambaut A" first="Andrew" last="Rambaut">Andrew Rambaut</name>
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