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Article: Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans

TitleTemporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans
Authors
KeywordsEvolution
Molecular epidemiology
Phylogeography
Source-sink
Issue Date2011
PublisherNational Academy of Sciences. The Journal's web site is located at http://www.pnas.org
Citation
Proceedings of the National Academy of Sciences of the United States of America, 2011, v. 108 n. 48, p. 19359-19364 How to Cite?
AbstractPopulations of seasonal influenza virus experience strong annual bottlenecks that pose a considerable extinction risk. It has been suggested that an influenza source population located in tropical Southeast or East Asia seeds annual temperate epidemics. Here we investigate the seasonal dynamics and migration patterns of influenza A H3N2 virus by analysis of virus samples obtained from 2003 to 2006 from Australia, Europe, Japan, New York, New Zealand, Southeast Asia, and newly sequenced viruses from Hong Kong. In contrast to annual temperate epidemics, relatively low levels of relative genetic diversity and no seasonal fluctuations characterized virus populations in tropical Southeast Asia and Hong Kong. Bayesian phylogeographic analysis using discrete temporal and spatial characters reveal high rates of viral migration between urban centers tested. Although the virus population that migrated between Southeast Asia and Hong Kong persisted through time, this was dependent on virus input from temperate regions and these tropical regions did not maintain a source for annual H3N2 influenza epidemics. We further show that multiple lineages may seed annual influenza epidemics, and that each region may function as a potential source population. We therefore propose that the global persistence of H3N2 influenza A virus is the result of a migrating metapopulation in which multiple different localities may seed seasonal epidemics in temperate regions in a given year. Such complex global migration dynamics may confound control efforts and contribute to the emergence and spread of antigenic variants and drug-resistant viruses.
Persistent Identifierhttp://hdl.handle.net/10722/151762
ISSN
2021 Impact Factor: 12.779
2020 SCImago Journal Rankings: 5.011
PubMed Central ID
ISI Accession Number ID
Funding AgencyGrant Number
National Institute of Allergy and Infectious Disease, National Institutes of Health, Department of Health and Human ServicesHHSN266200700005C
HHSN272200900007
Area of Excellence Scheme of the University Grants Committee of the Hong Kong Special Administrative Region Government
RAPIDD of the Science and Technology Directorate, US Department of Homeland Security
Fogarty International Center, National Institutes of Health under National Institute of Allergy and Infectious DiseasesHHSN266200700005C
Duke-National University of Singapore
Agency for Science, Technology and Research, Singapore
Ministry of Health, Singapore
Funding Information:

This study was supported by Contracts HHSN266200700005C and HHSN272200900007 for the Influenza Genome Sequencing Project of the National Institute of Allergy and Infectious Disease, National Institutes of Health, Department of Health and Human Services; the Area of Excellence Scheme of the University Grants Committee (Grant AoE/M-12/06) of the Hong Kong Special Administrative Region Government; the RAPIDD program of the Science and Technology Directorate, US Department of Homeland Security and the Fogarty International Center, National Institutes of Health (S. R.), a career development award under National Institute of Allergy and Infectious Diseases Contract HHSN266200700005C (to G.J.D.S.); and the Duke-National University of Singapore Signature Research Program funded by the Agency for Science, Technology and Research, Singapore, and the Ministry of Health, Singapore (J.B., D.V., and G.J.D.S.).

References

 

DC FieldValueLanguage
dc.contributor.authorBahl, Jen_HK
dc.contributor.authorNelson, MIen_HK
dc.contributor.authorChan, KHen_HK
dc.contributor.authorChen, Ren_HK
dc.contributor.authorVijaykrishna, Den_HK
dc.contributor.authorHalpin, RAen_HK
dc.contributor.authorStockwell, TBen_HK
dc.contributor.authorLin, Xen_HK
dc.contributor.authorWentworth, DEen_HK
dc.contributor.authorGhedin, Een_HK
dc.contributor.authorGuan, Yen_HK
dc.contributor.authorPeiris, JSMen_HK
dc.contributor.authorRiley, Sen_HK
dc.contributor.authorRambaut, Aen_HK
dc.contributor.authorHolmes, ECen_HK
dc.contributor.authorSmith, GJDen_HK
dc.date.accessioned2012-06-26T06:28:01Z-
dc.date.available2012-06-26T06:28:01Z-
dc.date.issued2011en_HK
dc.identifier.citationProceedings of the National Academy of Sciences of the United States of America, 2011, v. 108 n. 48, p. 19359-19364en_HK
dc.identifier.issn0027-8424en_HK
dc.identifier.urihttp://hdl.handle.net/10722/151762-
dc.description.abstractPopulations of seasonal influenza virus experience strong annual bottlenecks that pose a considerable extinction risk. It has been suggested that an influenza source population located in tropical Southeast or East Asia seeds annual temperate epidemics. Here we investigate the seasonal dynamics and migration patterns of influenza A H3N2 virus by analysis of virus samples obtained from 2003 to 2006 from Australia, Europe, Japan, New York, New Zealand, Southeast Asia, and newly sequenced viruses from Hong Kong. In contrast to annual temperate epidemics, relatively low levels of relative genetic diversity and no seasonal fluctuations characterized virus populations in tropical Southeast Asia and Hong Kong. Bayesian phylogeographic analysis using discrete temporal and spatial characters reveal high rates of viral migration between urban centers tested. Although the virus population that migrated between Southeast Asia and Hong Kong persisted through time, this was dependent on virus input from temperate regions and these tropical regions did not maintain a source for annual H3N2 influenza epidemics. We further show that multiple lineages may seed annual influenza epidemics, and that each region may function as a potential source population. We therefore propose that the global persistence of H3N2 influenza A virus is the result of a migrating metapopulation in which multiple different localities may seed seasonal epidemics in temperate regions in a given year. Such complex global migration dynamics may confound control efforts and contribute to the emergence and spread of antigenic variants and drug-resistant viruses.en_HK
dc.languageengen_US
dc.publisherNational Academy of Sciences. The Journal's web site is located at http://www.pnas.orgen_HK
dc.relation.ispartofProceedings of the National Academy of Sciences of the United States of Americaen_HK
dc.subjectEvolutionen_HK
dc.subjectMolecular epidemiologyen_HK
dc.subjectPhylogeographyen_HK
dc.subjectSource-sinken_HK
dc.subject.meshAsia - Epidemiologyen_US
dc.subject.meshAustralasia - Epidemiologyen_US
dc.subject.meshBase Sequenceen_US
dc.subject.meshBayes Theoremen_US
dc.subject.meshDemographyen_US
dc.subject.meshDisease Outbreaksen_US
dc.subject.meshEurope - Epidemiologyen_US
dc.subject.meshEvolution, Molecularen_US
dc.subject.meshGenetic Variationen_US
dc.subject.meshHumansen_US
dc.subject.meshInfluenza A Virus, H3n2 Subtype - Genetics - Physiologyen_US
dc.subject.meshInfluenza, Human - Epidemiologyen_US
dc.subject.meshModels, Biologicalen_US
dc.subject.meshModels, Geneticen_US
dc.subject.meshMolecular Sequence Dataen_US
dc.subject.meshNew York - Epidemiologyen_US
dc.subject.meshPhylogeographyen_US
dc.subject.meshPopulation Dynamicsen_US
dc.subject.meshReverse Transcriptase Polymerase Chain Reactionen_US
dc.subject.meshSeasonsen_US
dc.subject.meshSequence Analysis, Dnaen_US
dc.titleTemporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humansen_HK
dc.typeArticleen_HK
dc.identifier.emailGuan, Y: yguan@hkucc.hku.hken_HK
dc.identifier.emailPeiris, JSM: malik@hkucc.hku.hken_HK
dc.identifier.emailRiley, S: steven.riley@hku.hken_HK
dc.identifier.emailSmith, GJD: gjsmith@hkucc1.hku.hken_HK
dc.identifier.authorityGuan, Y=rp00397en_HK
dc.identifier.authorityPeiris, JSM=rp00410en_HK
dc.identifier.authorityRiley, S=rp00511en_HK
dc.identifier.authoritySmith, GJD=rp00444en_HK
dc.description.naturelink_to_OA_fulltexten_US
dc.identifier.doi10.1073/pnas.1109314108en_HK
dc.identifier.pmid22084096-
dc.identifier.pmcidPMC3228450-
dc.identifier.scopuseid_2-s2.0-82755190600en_HK
dc.identifier.hkuros211240-
dc.relation.referenceshttp://www.scopus.com/mlt/select.url?eid=2-s2.0-82755190600&selection=ref&src=s&origin=recordpageen_HK
dc.identifier.volume108en_HK
dc.identifier.issue48en_HK
dc.identifier.spage19359en_HK
dc.identifier.epage19364en_HK
dc.identifier.isiWOS:000297463100054-
dc.publisher.placeUnited Statesen_HK
dc.identifier.scopusauthoridBahl, J=35308668200en_HK
dc.identifier.scopusauthoridNelson, MI=15758216500en_HK
dc.identifier.scopusauthoridChan, KH=7406034307en_HK
dc.identifier.scopusauthoridChen, R=15060989600en_HK
dc.identifier.scopusauthoridVijaykrishna, D=12752817700en_HK
dc.identifier.scopusauthoridHalpin, RA=15822104200en_HK
dc.identifier.scopusauthoridStockwell, TB=16242581000en_HK
dc.identifier.scopusauthoridLin, X=36164400700en_HK
dc.identifier.scopusauthoridWentworth, DE=7004800841en_HK
dc.identifier.scopusauthoridGhedin, E=6602723755en_HK
dc.identifier.scopusauthoridGuan, Y=7202924055en_HK
dc.identifier.scopusauthoridPeiris, JSM=7005486823en_HK
dc.identifier.scopusauthoridRiley, S=7102619416en_HK
dc.identifier.scopusauthoridRambaut, A=7004230842en_HK
dc.identifier.scopusauthoridHolmes, EC=35433598300en_HK
dc.identifier.scopusauthoridSmith, GJD=8344015800en_HK
dc.identifier.citeulike10310004-
dc.identifier.issnl0027-8424-

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