Origins of the 2009 H1N1 influenza pandemic in swine in Mexico
Identifieur interne : 000090 ( Pmc/Curation ); précédent : 000089; suivant : 000091Origins of the 2009 H1N1 influenza pandemic in swine in Mexico
Auteurs : Ignacio Mena [États-Unis] ; Martha I. Nelson [États-Unis] ; Francisco Quezada-Monroy [Mexique] ; Jayeeta Dutta [États-Unis] ; Refugio Cortes-Fernández [Mexique] ; J Horacio Lara-Puente [Mexique] ; Felipa Castro-Peralta [Mexique] ; Luis F. Cunha [États-Unis] ; Nídia S. Trovão [États-Unis, Belgique] ; Bernardo Lozano-Dubernard [Mexique] ; Andrew Rambaut [États-Unis, Royaume-Uni] ; Harm Van Bakel [États-Unis] ; Adolfo García-Sastre [États-Unis]Source :
- eLife [ 2050-084X ] ; ????.
Abstract
Asia is considered an important source of influenza A virus (IAV) pandemics, owing to large, diverse viral reservoirs in poultry and swine. However, the zoonotic origins of the 2009 A/H1N1 influenza pandemic virus (pdmH1N1) remain unclear, due to conflicting evidence from swine and humans. There is strong evidence that the first human outbreak of pdmH1N1 occurred in Mexico in early 2009. However, no related swine viruses have been detected in Mexico or any part of the Americas, and to date the most closely related ancestor viruses were identified in Asian swine. Here, we use 58 new whole-genome sequences from IAVs collected in Mexican swine to establish that the swine virus responsible for the 2009 pandemic evolved in central Mexico. This finding highlights how the 2009 pandemic arose from a region not considered a pandemic risk, owing to an expansion of IAV diversity in swine resulting from long-distance live swine trade.
Url:
DOI: 10.7554/eLife.16777
PubMed: 27350259
PubMed Central: 4957980
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Origins of the 2009 H1N1 influenza pandemic in swine in Mexico</title>
<author><name sortKey="Mena, Ignacio" sort="Mena, Ignacio" uniqKey="Mena I" first="Ignacio" last="Mena">Ignacio Mena</name>
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<author><name sortKey="Quezada Monroy, Francisco" sort="Quezada Monroy, Francisco" uniqKey="Quezada Monroy F" first="Francisco" last="Quezada-Monroy">Francisco Quezada-Monroy</name>
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<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Dutta, Jayeeta" sort="Dutta, Jayeeta" uniqKey="Dutta J" first="Jayeeta" last="Dutta">Jayeeta Dutta</name>
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<author><name sortKey="Trovao, Nidia S" sort="Trovao, Nidia S" uniqKey="Trovao N" first="Nídia S" last="Trovão">Nídia S. Trovão</name>
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</nlm:aff>
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<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Lozano Dubernard, Bernardo" sort="Lozano Dubernard, Bernardo" uniqKey="Lozano Dubernard B" first="Bernardo" last="Lozano-Dubernard">Bernardo Lozano-Dubernard</name>
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<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Rambaut, Andrew" sort="Rambaut, Andrew" uniqKey="Rambaut A" first="Andrew" last="Rambaut">Andrew Rambaut</name>
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,<country>United States</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7"><institution content-type="dept">Institute of Evolutionary Biology</institution>
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,<addr-line>Edinburgh</addr-line>
,<country>United Kingdom</country>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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,<addr-line>Edinburgh</addr-line>
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</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Van Bakel, Harm" sort="Van Bakel, Harm" uniqKey="Van Bakel H" first="Harm" last="Van Bakel">Harm Van Bakel</name>
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</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Garcia Sastre, Adolfo" sort="Garcia Sastre, Adolfo" uniqKey="Garcia Sastre A" first="Adolfo" last="García-Sastre">Adolfo García-Sastre</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution content-type="dept">Department of Microbiology</institution>
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</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff9"><institution content-type="dept">Department of Medicine, Division of Infectious Diseases</institution>
,<institution>Icahn School of Medicine at Mount Sinai</institution>
,<addr-line>New York</addr-line>
,<country>United States</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">eLife</title>
<idno type="eISSN">2050-084X</idno>
<imprint><date when="????">????</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>Asia is considered an important source of influenza A virus (IAV) pandemics, owing to large, diverse viral reservoirs in poultry and swine. However, the zoonotic origins of the 2009 A/H1N1 influenza pandemic virus (pdmH1N1) remain unclear, due to conflicting evidence from swine and humans. There is strong evidence that the first human outbreak of pdmH1N1 occurred in Mexico in early 2009. However, no related swine viruses have been detected in Mexico or any part of the Americas, and to date the most closely related ancestor viruses were identified in Asian swine. Here, we use 58 new whole-genome sequences from IAVs collected in Mexican swine to establish that the swine virus responsible for the 2009 pandemic evolved in central Mexico. This finding highlights how the 2009 pandemic arose from a region not considered a pandemic risk, owing to an expansion of IAV diversity in swine resulting from long-distance live swine trade.</p>
<p><bold>DOI:</bold>
<ext-link ext-link-type="doi" xlink:href="10.7554/eLife.16777.001">http://dx.doi.org/10.7554/eLife.16777.001</ext-link>
</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">eLife</journal-id>
<journal-id journal-id-type="iso-abbrev">Elife</journal-id>
<journal-id journal-id-type="hwp">eLife</journal-id>
<journal-id journal-id-type="publisher-id">eLife</journal-id>
<journal-title-group><journal-title>eLife</journal-title>
</journal-title-group>
<issn pub-type="epub">2050-084X</issn>
<publisher><publisher-name>eLife Sciences Publications, Ltd</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27350259</article-id>
<article-id pub-id-type="pmc">4957980</article-id>
<article-id pub-id-type="publisher-id">16777</article-id>
<article-id pub-id-type="doi">10.7554/eLife.16777</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Epidemiology and Global Health</subject>
</subj-group>
<subj-group subj-group-type="heading"><subject>Microbiology and Infectious Disease</subject>
</subj-group>
<subj-group subj-group-type="display-channel"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Origins of the 2009 H1N1 influenza pandemic in swine in Mexico</article-title>
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<contrib-group><contrib id="author-55467" contrib-type="author"><name><surname>Mena</surname>
<given-names>Ignacio</given-names>
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<aff id="aff1"><label>1</label>
<institution content-type="dept">Department of Microbiology</institution>
,<institution>Icahn School of Medicine at Mount Sinai</institution>
,<addr-line>New York</addr-line>
,<country>United States</country>
</aff>
<aff id="aff2"><label>2</label>
<institution content-type="dept">Global Health and Emerging Pathogens Institute</institution>
,<institution>Icahn School of Medicine at Mount Sinai</institution>
,<addr-line>New York</addr-line>
,<country>United States</country>
</aff>
<aff id="aff3"><label>3</label>
<institution content-type="dept">Division of International Epidemiology and Population Studies, Fogarty International Center</institution>
,<institution>National Institutes of Health</institution>
,<addr-line>Bethesda</addr-line>
,<country>United States</country>
</aff>
<aff id="aff4"><label>4</label>
<institution>Laboratorio Avi-Mex</institution>
,<addr-line>Mexico City</addr-line>
,<country>Mexico</country>
</aff>
<aff id="aff5"><label>5</label>
<institution content-type="dept">Genetics and Genomic Sciences</institution>
,<institution>Icahn School of Medicine at Mount Sinai</institution>
,<addr-line>New York</addr-line>
,<country>United States</country>
</aff>
<aff id="aff6"><label>6</label>
<institution content-type="dept">Department of Microbiology and Immunology</institution>
,<institution>Rega Institute, University of Leuven</institution>
,<addr-line>Leuven</addr-line>
,<country>Belgium</country>
</aff>
<aff id="aff7"><label>7</label>
<institution content-type="dept">Institute of Evolutionary Biology</institution>
,<institution>University of Edinburgh</institution>
,<addr-line>Edinburgh</addr-line>
,<country>United Kingdom</country>
</aff>
<aff id="aff8"><label>8</label>
<institution content-type="dept">Centre for Immunology, Infection and Evolution</institution>
,<institution>University of Edinburgh</institution>
,<addr-line>Edinburgh</addr-line>
,<country>United Kingdom</country>
</aff>
<aff id="aff9"><label>9</label>
<institution content-type="dept">Department of Medicine, Division of Infectious Diseases</institution>
,<institution>Icahn School of Medicine at Mount Sinai</institution>
,<addr-line>New York</addr-line>
,<country>United States</country>
</aff>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Neher</surname>
<given-names>Richard A</given-names>
</name>
<aff id="aff10"><institution>Max Planck Institute for Developmental Biology</institution>
,<country>Germany</country>
</aff>
</contrib>
</contrib-group>
<author-notes><corresp id="cor1"><email>adolfo.garcia-sastre@mssm.edu</email>
</corresp>
<fn fn-type="con" id="equal-contrib"><label>†</label>
<p>These authors contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date date-type="pub" publication-format="electronic"><day>28</day>
<month>6</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<volume>5</volume>
<elocation-id>e16777</elocation-id>
<history><date date-type="received"><day>08</day>
<month>4</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>13</day>
<month>6</month>
<year>2016</year>
</date>
</history>
<permissions><license xlink:href="http://creativecommons.org/publicdomain/zero/1.0/"><license-p>This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">Creative Commons CC0 public domain dedication</ext-link>
.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="elife-16777.pdf"></self-uri>
<abstract><p>Asia is considered an important source of influenza A virus (IAV) pandemics, owing to large, diverse viral reservoirs in poultry and swine. However, the zoonotic origins of the 2009 A/H1N1 influenza pandemic virus (pdmH1N1) remain unclear, due to conflicting evidence from swine and humans. There is strong evidence that the first human outbreak of pdmH1N1 occurred in Mexico in early 2009. However, no related swine viruses have been detected in Mexico or any part of the Americas, and to date the most closely related ancestor viruses were identified in Asian swine. Here, we use 58 new whole-genome sequences from IAVs collected in Mexican swine to establish that the swine virus responsible for the 2009 pandemic evolved in central Mexico. This finding highlights how the 2009 pandemic arose from a region not considered a pandemic risk, owing to an expansion of IAV diversity in swine resulting from long-distance live swine trade.</p>
<p><bold>DOI:</bold>
<ext-link ext-link-type="doi" xlink:href="10.7554/eLife.16777.001">http://dx.doi.org/10.7554/eLife.16777.001</ext-link>
</p>
</abstract>
<abstract abstract-type="executive-summary"><title>eLife digest</title>
<p>In 2009 a new influenza virus jumped from pigs to humans and spread very rapidly, causing an initial outbreak in Mexico and becoming a global pandemic in just a few months. Although the most straightforward explanation is that the virus originated in swine in Mexico, several studies suggested that this was unlikely because key genetic components of the virus had never been detected in the Americas. Determining the source of the disease is critical for predicting and preparing for future influenza pandemics.</p>
<p>Mena, Nelson et al. sought to better characterize the genetic diversity of influenza viruses in Mexican swine by obtaining the entire genetic sequences of 58 viruses collected from swine in Mexico, including some from previously unsampled regions in central Mexico. The sequences revealed extensive diversity among the influenza viruses circulating in Mexican swine. Several viruses included genetic segments that originated from viruses from Eurasia (the landmass containing Europe and Asia) and had not previously been detected in the Americas. The new sequences contained key genetic components of the 2009 pandemic virus. Furthermore, the sequences suggest that viruses with a similar genetic composition to the 2009 pandemic virus have been circulating in pigs in central-west Mexico for more than a decade. Thus, this region is the most likely source of the virus that started the 2009 pandemic.</p>
<p>Mena, Nelson et al. also found that the movement of viruses from Eurasia and the United States into Mexico closely follows the direction of the global trade of live swine. This highlights the critical role that animal trading plays in bringing together diverse viruses from different continents, which can then combine and generate new pandemic viruses.</p>
<p>A potential next step is to perform experiments that investigate how well the swine viruses can replicate and pass between different animal models. Comparing the results of such experiments with the findings presented by Mena, Nelson et al. could identify factors that make the viruses more likely to spread to humans and produce a pandemic.</p>
<p><bold>DOI:</bold>
<ext-link ext-link-type="doi" xlink:href="10.7554/eLife.16777.002">http://dx.doi.org/10.7554/eLife.16777.002</ext-link>
</p>
</abstract>
<kwd-group kwd-group-type="author-keywords"><title>Author Keywords</title>
<kwd>influenza A virus</kwd>
<kwd>2009 pandemic</kwd>
<kwd>swine</kwd>
<kwd>evolution</kwd>
<kwd>zoonosis</kwd>
<kwd>phylogeography</kwd>
</kwd-group>
<kwd-group kwd-group-type="research-organism"><title>Research Organism</title>
<kwd>Virus</kwd>
</kwd-group>
<funding-group><award-group id="par-1"><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/100000002</institution-id>
<institution>National Institutes of Health</institution>
</institution-wrap>
</funding-source>
<award-id>Centers of Excellence for Influenza Research and Surveillance, Contract No.HHSN272201400008C</award-id>
<principal-award-recipient><name><surname>García-Sastre</surname>
<given-names>Adolfo</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="par-2"><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/100000061</institution-id>
<institution>Fogarty International Center</institution>
</institution-wrap>
</funding-source>
<award-id>Multinational Influenza Seasonal Mortality Study</award-id>
<principal-award-recipient><name><surname>Nelson</surname>
<given-names>Martha I</given-names>
</name>
</principal-award-recipient>
</award-group>
<funding-statement>The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.</funding-statement>
</funding-group>
<custom-meta-group><custom-meta><meta-name>elife-xml-version</meta-name>
<meta-value>2.5</meta-value>
</custom-meta>
<custom-meta specific-use="meta-only"><meta-name>Author impact statement</meta-name>
<meta-value>Genome sequence data from 58 Mexican swine influenza A viruses resolves the spatial origin of the virus that originated the influenza pandemic of 2009.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
<sub-article id="SA1" article-type="article-commentary"><front-stub><article-id pub-id-type="doi">10.7554/eLife.16777.034</article-id>
<title-group><article-title>Decision letter</article-title>
</title-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Neher</surname>
<given-names>Richard A</given-names>
</name>
<aff id="aff11"><institution>Max Planck Institute for Developmental Biology</institution>
,<country>Germany</country>
</aff>
</contrib>
</contrib-group>
</front-stub>
<body><boxed-text position="float" orientation="portrait"><p>In the interests of transparency, eLife includes the editorial decision letter and accompanying author responses. A lightly edited version of the letter sent to the authors after peer review is shown, indicating the most substantive concerns; minor comments are not usually included.</p>
</boxed-text>
<p>Thank you for submitting your article "Origins of the 2009 H1N1 influenza pandemic in swine in Mexico" for consideration by <italic>eLife</italic>
. Your article has been reviewed by three peer reviewers, one of whom is a member of our Board of Reviewing Editors and the evaluation has been overseen by Arup Chakraborty as the Senior Editor. The reviewers have opted to remain anonymous.</p>
<p>The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission.</p>
<p>Summary:</p>
<p>The manuscript presents a phylogenetic analysis of 58 full influenza A virus genomes collected from swine in Mexico to shed light on the origin of the 2009 pandemic of H1N1 influenza. The newly sequenced genomes close important gaps in our understanding of the emergence of this pandemic. The authors show that virus variants with sequences closely related to all segments of human H1N1pdm09 circulate in Mexican swine. This finding singles out Mexico as the likely region where the pandemic virus emerged. These results emphasize the need for concerted global surveillance of influenza virus diversity in animals.</p>
<p>All reviewers agree that the data shed light on an important and interesting problem. However, before we can recommend acceptance, a number of issues should be addressed.</p>
<p>Essential revisions:</p>
<p>1) More details on sample collection: How many samples were tested in different years? How were animals chosen for testing? Did these animals come from large commercial facilities or backyard farms? What were the criteria for sequencing positive samples? Within each location (Sonora, Puebla, etc) did the samples consistently come from the same producers/farms?</p>
<p>2) We would like to see a more extensive discussion of the gaps in surveillance in swine (not only in Mexico, but also Asia and Europe), and how these gaps limit the inferences that can be made.</p>
</body>
</sub-article>
<sub-article id="SA2" article-type="reply"><front-stub><article-id pub-id-type="doi">10.7554/eLife.16777.035</article-id>
<title-group><article-title>Author response</article-title>
</title-group>
</front-stub>
<body><p>Essential revisions:</p>
<p>1) More details on sample collection: How many samples were tested in different years? How were animals chosen for testing? Did these animals come from large commercial facilities or backyard farms? What were the criteria for sequencing positive samples? Within each location (Sonora, Puebla, etc) did the samples consistently come from the same producers/farms?</p>
<p>Following the reviewers’ suggestions, we have extended the description of the sample collection and virus isolation in the Materials and Materials and methods section to include all the information requested by the reviewers. The revised paragraph is:</p>
<p>“Collection of influenza viruses in Mexican swine. Swine influenza isolates were obtained from samples submitted to Avimex laboratories (Mexico) for routine confirmation diagnostics of pigs with respiratory syndrome. […] GenBank accession numbers of the 58 genomes are available in the Dryad data repository under DOI: 10.5061/dryad.m550m. Figure 2—figure supplement 1 describes the date, location, subtype and lineage assignment of each viral segment.”</p>
<p>2) We would like to see a more extensive discussion of the gaps in surveillance in swine (not only in Mexico, but also Asia and Europe), and how these gaps limit the inferences that can be made.</p>
<p>This is a very important issue, and our revised manuscript addressed this matter in further detail in the Results and the Discussion. We have also changed many of our references from ‘European swine’ to ‘Eurasian swine’ to better reflect ambiguities about the source Eurasian viruses in Mexico.</p>
<p>Results; “We also recognize the need to draw phylogeographic inferences with an awareness of missing data. Major gaps in surveillance in swine in Europe and Asia during the 1990s have resulted in long branch lengths between swIAVs collected in Mexico and Eurasia (<xref ref-type="fig" rid="fig3s1">Figure 3—figure supplement 1</xref>
). Although it is difficult to infer from the tree whether the EAsw MP identified in Mexico was introduced from Asian or European swine (<xref ref-type="fig" rid="fig4s1">Figure 4—figure supplement 1</xref>
), the lack of live swine imports reported between Mexico and any Asian country (<xref ref-type="fig" rid="fig6">Figure 6</xref>
), and the low export of Asian swine globally (Nelson et al., 2015c) suggest that Europe may be a more likely source of the Mexican viruses, similar to the H1 and N1 segments.”</p>
<p>Discussion; “At this time we cannot rule out Asia-to-Mexico viral migration, owing to possible omissions in reported imports and exports of swine and gaps in sequencing of viruses in swine globally. […] Globally, Asia is overwhelmingly a net importer of swine from Europe and North America, with extremely little export of Asian pigs or their viruses to any other continents (Nelson et al., 2015c).”</p>
</body>
</sub-article>
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