Frequency of influenza H3N2 intra-subtype reassortment: attributes and implications of reassortant spread
Identifieur interne : 000453 ( Main/Exploration ); précédent : 000452; suivant : 000454Frequency 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
Affiliations:
- Corée du Sud, Pérou, Thaïlande, États-Unis
- Californie, District de Columbia, Maryland, Région capitale de Séoul
- Séoul
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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. 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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><wicri:noRegion>Lima</wicri:noRegion></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><wicri:noRegion>Lima</wicri:noRegion></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><wicri:noRegion>Bangkok</wicri:noRegion></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><wicri:noRegion>Bangkok</wicri:noRegion></affiliation><affiliation wicri:level="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></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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Neumann</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Martin, D" uniqKey="Martin D">D Martin</name></author><author><name sortKey="Rybicki, E" uniqKey="Rybicki E">E Rybicki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Padidam, M" uniqKey="Padidam M">M Padidam</name></author><author><name sortKey="Sawyer, S" uniqKey="Sawyer S">S Sawyer</name></author><author><name sortKey="Fauquet, Cm" uniqKey="Fauquet C">CM Fauquet</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Salminen, Mo" uniqKey="Salminen M">MO Salminen</name></author><author><name sortKey="Carr, Jk" uniqKey="Carr J">JK Carr</name></author><author><name sortKey="Burke, Ds" uniqKey="Burke D">DS Burke</name></author><author><name sortKey="Mccutchan, Fe" uniqKey="Mccutchan F">FE McCutchan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Smith, Jm" uniqKey="Smith J">JM Smith</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Posada, D" uniqKey="Posada D">D Posada</name></author><author><name sortKey="Crandall, Ka" uniqKey="Crandall K">KA Crandall</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gibbs, Mj" uniqKey="Gibbs M">MJ Gibbs</name></author><author><name sortKey="Armstrong, Js" uniqKey="Armstrong J">JS Armstrong</name></author><author><name sortKey="Gibbs, Aj" uniqKey="Gibbs A">AJ Gibbs</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Weiller, Gf" uniqKey="Weiller G">GF Weiller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Holmes, Ec" uniqKey="Holmes E">EC Holmes</name></author><author><name sortKey="Worobey, M" uniqKey="Worobey M">M Worobey</name></author><author><name sortKey="Rambaut, A" uniqKey="Rambaut A">A Rambaut</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Boni, Mf" uniqKey="Boni M">MF Boni</name></author><author><name sortKey="Posada, D" uniqKey="Posada D">D Posada</name></author><author><name sortKey="Feldman, Mw" uniqKey="Feldman M">MW Feldman</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Corée du Sud</li><li>Pérou</li><li>Thaïlande</li><li>États-Unis</li></country><region><li>Californie</li><li>District de Columbia</li><li>Maryland</li><li>Région capitale de Séoul</li></region><settlement><li>Séoul</li></settlement></list><tree><country name="États-Unis"><region name="Maryland"><name sortKey="Maljkovic Berry, Irina" sort="Maljkovic Berry, Irina" uniqKey="Maljkovic Berry I" first="Irina" last="Maljkovic Berry">Irina Maljkovic Berry</name></region><name sortKey="Blair, Patrick J" sort="Blair, Patrick J" uniqKey="Blair P" first="Patrick J." last="Blair">Patrick J. Blair</name><name sortKey="Brice, Gary T" sort="Brice, Gary T" uniqKey="Brice G" first="Gary T." last="Brice">Gary T. Brice</name><name sortKey="Edwards, Leslie D" sort="Edwards, Leslie D" uniqKey="Edwards L" first="Leslie D." last="Edwards">Leslie D. Edwards</name><name sortKey="Hawksworth, Anthony W" sort="Hawksworth, Anthony W" uniqKey="Hawksworth A" first="Anthony W." last="Hawksworth">Anthony W. Hawksworth</name><name sortKey="Jarman, Richard G" sort="Jarman, Richard G" uniqKey="Jarman R" first="Richard G." last="Jarman">Richard G. Jarman</name><name sortKey="Kuschner, Robert" sort="Kuschner, Robert" uniqKey="Kuschner R" first="Robert" last="Kuschner">Robert Kuschner</name><name sortKey="Li, Tao" sort="Li, Tao" uniqKey="Li T" first="Tao" last="Li">Tao Li</name><name sortKey="Lin, Xiaoxu" sort="Lin, Xiaoxu" uniqKey="Lin X" first="Xiaoxu" last="Lin">Xiaoxu Lin</name><name sortKey="Melendrez, Melanie C" sort="Melendrez, Melanie C" uniqKey="Melendrez M" first="Melanie C." last="Melendrez">Melanie C. Melendrez</name><name sortKey="Thomas, Stephen J" sort="Thomas, Stephen J" uniqKey="Thomas S" first="Stephen J." last="Thomas">Stephen J. Thomas</name></country><country name="Pérou"><noRegion><name sortKey="Halsey, Eric S" sort="Halsey, Eric S" uniqKey="Halsey E" first="Eric S." last="Halsey">Eric S. Halsey</name></noRegion><name sortKey="Williams, Maya" sort="Williams, Maya" uniqKey="Williams M" first="Maya" last="Williams">Maya Williams</name></country><country name="Thaïlande"><noRegion><name sortKey="Fernandez, Stefan" sort="Fernandez, Stefan" uniqKey="Fernandez S" first="Stefan" last="Fernandez">Stefan Fernandez</name></noRegion><name sortKey="Yoon, In Kyu" sort="Yoon, In Kyu" uniqKey="Yoon I" first="In-Kyu" last="Yoon">In-Kyu Yoon</name></country><country name="Corée du Sud"><region name="Région capitale de Séoul"><name sortKey="Yoon, In Kyu" sort="Yoon, In Kyu" uniqKey="Yoon I" first="In-Kyu" last="Yoon">In-Kyu Yoon</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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