Frequency of influenza H3N2 intra-subtype reassortment: attributes and implications of reassortant spread
Identifieur interne : 000153 ( Pmc/Curation ); précédent : 000152; suivant : 000154Frequency of influenza H3N2 intra-subtype reassortment: attributes and implications of reassortant spread
Auteurs : Irina Maljkovic Berry [États-Unis] ; Melanie C. Melendrez [États-Unis] ; Tao Li [États-Unis] ; Anthony W. Hawksworth [États-Unis] ; Gary T. Brice [États-Unis] ; Patrick J. Blair [États-Unis] ; Eric S. Halsey [Pérou] ; Maya Williams [Pérou] ; Stefan Fernandez [Thaïlande] ; In-Kyu Yoon [Thaïlande, Corée du Sud] ; Leslie D. Edwards [États-Unis] ; Robert Kuschner [États-Unis] ; Xiaoxu Lin [États-Unis] ; Stephen J. Thomas [États-Unis] ; Richard G. Jarman [États-Unis]Source :
- BMC Biology [ 1741-7007 ] ; 2016.
Abstract
Increasing evidence suggests that influenza reassortment not only contributes to the emergence of new human pandemics but also plays an important role in seasonal influenza epidemics, disease severity, evolution, and vaccine efficacy. We studied this process within 2091 H3N2 full genomes utilizing a combination of the latest reassortment detection tools and more conventional phylogenetic analyses.
We found that the amount of H3N2 intra-subtype reassortment depended on the number of sampled genomes, occurred with a steady frequency of 3.35%, and was not affected by the geographical origins, evolutionary patterns, or previous reassortment history of the virus. We identified both single reassortant genomes and reassortant clades, each clade representing one reassortment event followed by successful spread of the reassorted variant in the human population. It was this spread that was mainly responsible for the observed high presence of H3N2 intra-subtype reassortant genomes. The successfully spread variants were generally sampled within one year of their formation, highlighting the risk of their rapid spread but also presenting an opportunity for their rapid detection. Simultaneous spread of several different reassortant lineages was observed, and despite their limited average lifetime, second and third generation reassortment was detected, as well as reassortment between viruses belonging to different vaccine-associated clades, likely displaying differing antigenic properties. Some of the spreading reassortants remained confined to certain geographical regions, while others, sharing common properties in amino acid positions of the HA, NA, and PB2 segments, were found throughout the world.
Detailed surveillance of seasonal influenza reassortment patterns and variant properties may provide unique information needed for prediction of spread and construction of future influenza vaccines.
The online version of this article (doi:10.1186/s12915-016-0337-3) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s12915-016-0337-3
PubMed: 28034300
PubMed Central: 5200972
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Edwards</name><affiliation wicri:level="2"><nlm:aff id="Aff5">Office of Medical Services, US Department of State, Washington, DC USA</nlm:aff><country>États-Unis</country><placeName><region type="state">District de Columbia</region></placeName><wicri:cityArea>Office of Medical Services, US Department of State, Washington</wicri:cityArea></affiliation></author><author><name sortKey="Kuschner, Robert" sort="Kuschner, Robert" uniqKey="Kuschner R" first="Robert" last="Kuschner">Robert Kuschner</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author><author><name sortKey="Lin, Xiaoxu" sort="Lin, Xiaoxu" uniqKey="Lin X" first="Xiaoxu" last="Lin">Xiaoxu Lin</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author><author><name sortKey="Thomas, Stephen J" sort="Thomas, Stephen J" uniqKey="Thomas S" first="Stephen J." last="Thomas">Stephen J. Thomas</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author><author><name sortKey="Jarman, Richard G" sort="Jarman, Richard G" uniqKey="Jarman R" first="Richard G." last="Jarman">Richard G. Jarman</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28034300</idno><idno type="pmc">5200972</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5200972</idno><idno type="RBID">PMC:5200972</idno><idno type="doi">10.1186/s12915-016-0337-3</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000153</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000153</idno><idno type="wicri:Area/Pmc/Curation">000153</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000153</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Frequency of influenza H3N2 intra-subtype reassortment: attributes and implications of reassortant spread</title><author><name sortKey="Maljkovic Berry, Irina" sort="Maljkovic Berry, Irina" uniqKey="Maljkovic Berry I" first="Irina" last="Maljkovic Berry">Irina Maljkovic Berry</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author><author><name sortKey="Melendrez, Melanie C" sort="Melendrez, Melanie C" uniqKey="Melendrez M" first="Melanie C." last="Melendrez">Melanie C. Melendrez</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author><author><name sortKey="Li, Tao" sort="Li, Tao" uniqKey="Li T" first="Tao" last="Li">Tao Li</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author><author><name sortKey="Hawksworth, Anthony W" sort="Hawksworth, Anthony W" uniqKey="Hawksworth A" first="Anthony W." last="Hawksworth">Anthony W. Hawksworth</name><affiliation wicri:level="2"><nlm:aff id="Aff2">Operational Infectious Diseases Directorate, Naval Health Research Center, San Diego, CA USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Operational Infectious Diseases Directorate, Naval Health Research Center, San Diego</wicri:cityArea></affiliation></author><author><name sortKey="Brice, Gary T" sort="Brice, Gary T" uniqKey="Brice G" first="Gary T." last="Brice">Gary T. Brice</name><affiliation wicri:level="2"><nlm:aff id="Aff2">Operational Infectious Diseases Directorate, Naval Health Research Center, San Diego, CA USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Operational Infectious Diseases Directorate, Naval Health Research Center, San Diego</wicri:cityArea></affiliation></author><author><name sortKey="Blair, Patrick J" sort="Blair, Patrick J" uniqKey="Blair P" first="Patrick J." last="Blair">Patrick J. Blair</name><affiliation wicri:level="2"><nlm:aff id="Aff2">Operational Infectious Diseases Directorate, Naval Health Research Center, San Diego, CA USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Operational Infectious Diseases Directorate, Naval Health Research Center, San Diego</wicri:cityArea></affiliation></author><author><name sortKey="Halsey, Eric S" sort="Halsey, Eric S" uniqKey="Halsey E" first="Eric S." last="Halsey">Eric S. Halsey</name><affiliation wicri:level="1"><nlm:aff id="Aff3">US Naval Medical Research Unit −6, Lima, Peru</nlm:aff><country xml:lang="fr">Pérou</country><wicri:regionArea>US Naval Medical Research Unit −6, Lima</wicri:regionArea></affiliation></author><author><name sortKey="Williams, Maya" sort="Williams, Maya" uniqKey="Williams M" first="Maya" last="Williams">Maya Williams</name><affiliation wicri:level="1"><nlm:aff id="Aff3">US Naval Medical Research Unit −6, Lima, Peru</nlm:aff><country xml:lang="fr">Pérou</country><wicri:regionArea>US Naval Medical Research Unit −6, Lima</wicri:regionArea></affiliation></author><author><name sortKey="Fernandez, Stefan" sort="Fernandez, Stefan" uniqKey="Fernandez S" first="Stefan" last="Fernandez">Stefan Fernandez</name><affiliation wicri:level="1"><nlm:aff id="Aff4">Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand</nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Armed Forces Research Institute of Medical Sciences, Bangkok</wicri:regionArea></affiliation></author><author><name sortKey="Yoon, In Kyu" sort="Yoon, In Kyu" uniqKey="Yoon I" first="In-Kyu" last="Yoon">In-Kyu Yoon</name><affiliation wicri:level="1"><nlm:aff id="Aff4">Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand</nlm:aff><country xml:lang="fr">Thaïlande</country><wicri:regionArea>Armed Forces Research Institute of Medical Sciences, Bangkok</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff6">Present Address: International Vaccine Institute, Seoul, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Present Address: International Vaccine Institute, Seoul</wicri:regionArea></affiliation></author><author><name sortKey="Edwards, Leslie D" sort="Edwards, Leslie D" uniqKey="Edwards L" first="Leslie D." last="Edwards">Leslie D. Edwards</name><affiliation wicri:level="2"><nlm:aff id="Aff5">Office of Medical Services, US Department of State, Washington, DC USA</nlm:aff><country>États-Unis</country><placeName><region type="state">District de Columbia</region></placeName><wicri:cityArea>Office of Medical Services, US Department of State, Washington</wicri:cityArea></affiliation></author><author><name sortKey="Kuschner, Robert" sort="Kuschner, Robert" uniqKey="Kuschner R" first="Robert" last="Kuschner">Robert Kuschner</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author><author><name sortKey="Lin, Xiaoxu" sort="Lin, Xiaoxu" uniqKey="Lin X" first="Xiaoxu" last="Lin">Xiaoxu Lin</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author><author><name sortKey="Thomas, Stephen J" sort="Thomas, Stephen J" uniqKey="Thomas S" first="Stephen J." last="Thomas">Stephen J. Thomas</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author><author><name sortKey="Jarman, Richard G" sort="Jarman, Richard G" uniqKey="Jarman R" first="Richard G." last="Jarman">Richard G. Jarman</name><affiliation wicri:level="2"><nlm:aff id="Aff1">Walter Reed Army Institute of Research, Silver Spring, MD USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Walter Reed Army Institute of Research, Silver Spring</wicri:cityArea></affiliation></author></analytic><series><title level="j">BMC Biology</title><idno type="eISSN">1741-7007</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Increasing evidence suggests that influenza reassortment not only contributes to the emergence of new human pandemics but also plays an important role in seasonal influenza epidemics, disease severity, evolution, and vaccine efficacy. We studied this process within 2091 H3N2 full genomes utilizing a combination of the latest reassortment detection tools and more conventional phylogenetic analyses.</p></sec><sec><title>Results</title><p>We found that the amount of H3N2 intra-subtype reassortment depended on the number of sampled genomes, occurred with a steady frequency of 3.35%, and was not affected by the geographical origins, evolutionary patterns, or previous reassortment history of the virus. We identified both single reassortant genomes and reassortant clades, each clade representing one reassortment event followed by successful spread of the reassorted variant in the human population. It was this spread that was mainly responsible for the observed high presence of H3N2 intra-subtype reassortant genomes. The successfully spread variants were generally sampled within one year of their formation, highlighting the risk of their rapid spread but also presenting an opportunity for their rapid detection. Simultaneous spread of several different reassortant lineages was observed, and despite their limited average lifetime, second and third generation reassortment was detected, as well as reassortment between viruses belonging to different vaccine-associated clades, likely displaying differing antigenic properties. Some of the spreading reassortants remained confined to certain geographical regions, while others, sharing common properties in amino acid positions of the HA, NA, and PB2 segments, were found throughout the world.</p></sec><sec><title>Conclusions</title><p>Detailed surveillance of seasonal influenza reassortment patterns and variant properties may provide unique information needed for prediction of spread and construction of future influenza vaccines.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s12915-016-0337-3) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Scholtissek, C" uniqKey="Scholtissek C">C Scholtissek</name></author><author><name sortKey="Rohde, W" uniqKey="Rohde W">W Rohde</name></author><author><name sortKey="Von Hoyningen, V" uniqKey="Von 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<front><journal-meta><journal-id journal-id-type="nlm-ta">BMC Biol</journal-id><journal-id journal-id-type="iso-abbrev">BMC Biol</journal-id><journal-title-group><journal-title>BMC Biology</journal-title></journal-title-group><issn pub-type="epub">1741-7007</issn><publisher><publisher-name>BioMed Central</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28034300</article-id><article-id pub-id-type="pmc">5200972</article-id><article-id pub-id-type="publisher-id">337</article-id><article-id pub-id-type="doi">10.1186/s12915-016-0337-3</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Frequency of influenza H3N2 intra-subtype reassortment: attributes and implications of reassortant spread</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Maljkovic Berry</surname><given-names>Irina</given-names></name><address><email>irina.maljkovicberry.ctr@mail.mil</email></address><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Melendrez</surname><given-names>Melanie C.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Tao</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Hawksworth</surname><given-names>Anthony W.</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Brice</surname><given-names>Gary T.</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Blair</surname><given-names>Patrick J.</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Halsey</surname><given-names>Eric S.</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Williams</surname><given-names>Maya</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Fernandez</surname><given-names>Stefan</given-names></name><xref ref-type="aff" rid="Aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Yoon</surname><given-names>In-Kyu</given-names></name><xref ref-type="aff" rid="Aff4">4</xref><xref ref-type="aff" rid="Aff6">6</xref></contrib><contrib contrib-type="author"><name><surname>Edwards</surname><given-names>Leslie D.</given-names></name><xref ref-type="aff" rid="Aff5">5</xref></contrib><contrib contrib-type="author"><name><surname>Kuschner</surname><given-names>Robert</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Lin</surname><given-names>Xiaoxu</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Thomas</surname><given-names>Stephen J.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Jarman</surname><given-names>Richard G.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><aff id="Aff1"><label>1</label>Walter Reed Army Institute of Research, Silver Spring, MD USA</aff><aff id="Aff2"><label>2</label>Operational Infectious Diseases Directorate, Naval Health Research Center, San Diego, CA USA</aff><aff id="Aff3"><label>3</label>US Naval Medical Research Unit −6, Lima, Peru</aff><aff id="Aff4"><label>4</label>Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand</aff><aff id="Aff5"><label>5</label>Office of Medical Services, US Department of State, Washington, DC USA</aff><aff id="Aff6"><label>6</label>Present Address: International Vaccine Institute, Seoul, Republic of Korea</aff></contrib-group><pub-date pub-type="epub"><day>29</day><month>12</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>29</day><month>12</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>14</volume><elocation-id>117</elocation-id><history><date date-type="received"><day>4</day><month>8</month><year>2016</year></date><date date-type="accepted"><day>3</day><month>12</month><year>2016</year></date></history><permissions><copyright-statement>© The Author(s). 2016</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold>This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>) applies to the data made available in this article, unless otherwise stated.</license-p></license></permissions><abstract id="Abs1"><sec><title>Background</title><p>Increasing evidence suggests that influenza reassortment not only contributes to the emergence of new human pandemics but also plays an important role in seasonal influenza epidemics, disease severity, evolution, and vaccine efficacy. We studied this process within 2091 H3N2 full genomes utilizing a combination of the latest reassortment detection tools and more conventional phylogenetic analyses.</p></sec><sec><title>Results</title><p>We found that the amount of H3N2 intra-subtype reassortment depended on the number of sampled genomes, occurred with a steady frequency of 3.35%, and was not affected by the geographical origins, evolutionary patterns, or previous reassortment history of the virus. We identified both single reassortant genomes and reassortant clades, each clade representing one reassortment event followed by successful spread of the reassorted variant in the human population. It was this spread that was mainly responsible for the observed high presence of H3N2 intra-subtype reassortant genomes. The successfully spread variants were generally sampled within one year of their formation, highlighting the risk of their rapid spread but also presenting an opportunity for their rapid detection. Simultaneous spread of several different reassortant lineages was observed, and despite their limited average lifetime, second and third generation reassortment was detected, as well as reassortment between viruses belonging to different vaccine-associated clades, likely displaying differing antigenic properties. Some of the spreading reassortants remained confined to certain geographical regions, while others, sharing common properties in amino acid positions of the HA, NA, and PB2 segments, were found throughout the world.</p></sec><sec><title>Conclusions</title><p>Detailed surveillance of seasonal influenza reassortment patterns and variant properties may provide unique information needed for prediction of spread and construction of future influenza vaccines.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s12915-016-0337-3) contains supplementary material, which is available to authorized users.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Influenza</kwd><kwd>Reassortment</kwd><kwd>H3N2</kwd><kwd>Spread</kwd></kwd-group><funding-group><award-group><funding-source><institution>Global Emerging Infections Surveillance and Response System (GEIS), a Division of the Armed Forces Health Surveillance Center</institution></funding-source><award-id>P0172_15_WR</award-id><principal-award-recipient><name><surname>Jarman</surname><given-names>Richard G.</given-names></name></principal-award-recipient></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2016</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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