title: Global circulation patterns of seasonal influenza viruses vary with antigenic drift.
abstract: Understanding the spatiotemporal patterns of emergence and circulation of new human seasonal influenza virus variants is a key scientific and public health challenge. The global circulation patterns of influenza A/H3N2 viruses are well characterized, but the patterns of A/H1N1 and B viruses have remained largely unexplored. Here we show that the global circulation patterns of A/H1N1 (up to 2009), B/Victoria, and B/Yamagata viruses differ substantially from those of A/H3N2 viruses, on the basis of analyses of 9,604 haemagglutinin sequences of human seasonal influenza viruses from 2000 to 2012. Whereas genetic variants of A/H3N2 viruses did not persist locally between epidemics and were reseeded from East and Southeast Asia, genetic variants of A/H1N1 and B viruses persisted across several seasons and exhibited complex global dynamics with East and Southeast Asia playing a limited role in disseminating new variants. The less frequent global movement of influenza A/H1N1 and B viruses coincided with slower rates of antigenic evolution, lower ages of infection, and smaller, less frequent epidemics compared to A/H3N2 viruses. Detailed epidemic models support differences in age of infection, combined with the less frequent travel of children, as probable drivers of the differences in the patterns of global circulation, suggesting a complex interaction between virus evolution, epidemiology, and human behaviour.
authors.affiliation: Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA.
authors.forename: Trevor
authors.initials: T
authors.lastname: Bedford
authors.affiliation: 1] MRC Centre for Outbreak Analysis and Modelling, Department of Infectious Disease Epidemiology, School of Public Health, Imperial College London, London SW7 2AZ, UK [2] Fogarty International Center, National Institutes of Health, Bethesda, Maryland 20892, USA.
authors.forename: Steven
authors.initials: S
authors.lastname: Riley
authors.affiliation: World Health Organization (WHO) Collaborating Centre for Reference and Research on Influenza, Melbourne, Victoria 3000, Australia.
authors.forename: Ian G
authors.initials: IG
authors.lastname: Barr
authors.affiliation: SGT Medical College, Hospital and Research Institute, Village Budhera, District Gurgaon, Haryana 122505, India.
authors.forename: Shobha
authors.initials: S
authors.lastname: Broor
authors.affiliation: National Institute of Virology, Pune 411001, India.
authors.forename: Mandeep
authors.initials: M
authors.lastname: Chadha
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, Centers for Disease Control and Prevention, Atlanta, Georgia 30329, USA.
authors.forename: Nancy J
authors.initials: NJ
authors.lastname: Cox
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, Medical Research Council National Institute for Medical Research (NIMR), London NW7 1AA, UK.
authors.forename: Rodney S
authors.initials: RS
authors.lastname: Daniels
authors.affiliation: King Institute of Preventive Medicine and Research, Guindy, Chennai 600032, India.
authors.forename: C Palani
authors.initials: CP
authors.lastname: Gunasekaran
authors.affiliation: 1] World Health Organization (WHO) Collaborating Centre for Reference and Research on Influenza, Melbourne, Victoria 3000, Australia [2] Melbourne School of Population and Global Health, University of Melbourne, Parkville, Victoria 3010, Australia.
authors.forename: Aeron C
authors.initials: AC
authors.lastname: Hurt
authors.affiliation: World Health Organization (WHO) Collaborating Centre for Reference and Research on Influenza, Melbourne, Victoria 3000, Australia.
authors.forename: Anne
authors.initials: A
authors.lastname: Kelso
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, Centers for Disease Control and Prevention, Atlanta, Georgia 30329, USA.
authors.forename: Alexander
authors.initials: A
authors.lastname: Klimov
authors.affiliation: Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.
authors.forename: Nicola S
authors.initials: NS
authors.lastname: Lewis
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, National Institute for Viral Disease Control and Prevention, China CDC, Beijing 102206, China.
authors.forename: Xiyan
authors.initials: X
authors.lastname: Li
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, Medical Research Council National Institute for Medical Research (NIMR), London NW7 1AA, UK.
authors.forename: John W
authors.initials: JW
authors.lastname: McCauley
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, National Institute of Infectious Diseases, Tokyo 208-0011, Japan.
authors.forename: Takato
authors.initials: T
authors.lastname: Odagiri
authors.affiliation: National Institute of Virology, Pune 411001, India.
authors.forename: Varsha
authors.initials: V
authors.lastname: Potdar
authors.affiliation: 1] Fogarty International Center, National Institutes of Health, Bethesda, Maryland 20892, USA [2] Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK [3] Centre for Immunology, Infection and Evolution, University of Edinburgh, Edinburgh EH9 3FL, UK.
authors.forename: Andrew
authors.initials: A
authors.lastname: Rambaut
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, National Institute for Viral Disease Control and Prevention, China CDC, Beijing 102206, China.
authors.forename: Yuelong
authors.initials: Y
authors.lastname: Shu
authors.affiliation: Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.
authors.forename: Eugene
authors.initials: E
authors.lastname: Skepner
authors.affiliation: 1] Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK [2] Department of Viroscience, Erasmus Medical Center, 3015 Rotterdam, The Netherlands.
authors.forename: Derek J
authors.initials: DJ
authors.lastname: Smith
authors.affiliation: 1] Department of Biostatistics, UCLA Fielding School of Public Health, University of California, Los Angeles, California 90095, USA [2] Department of Biomathematics, David Geffen School of Medicine at UCLA, University of California, Los Angeles, California 90095, USA [3] Department of Human Genetics, David Geffen School of Medicine at UCLA, University of California, Los Angeles, California 90095, USA.
authors.forename: Marc A
authors.initials: MA
authors.lastname: Suchard
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, National Institute of Infectious Diseases, Tokyo 208-0011, Japan.
authors.forename: Masato
authors.initials: M
authors.lastname: Tashiro
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, National Institute for Viral Disease Control and Prevention, China CDC, Beijing 102206, China.
authors.forename: Dayan
authors.initials: D
authors.lastname: Wang
authors.affiliation: WHO Collaborating Center for Reference and Research on Influenza, Centers for Disease Control and Prevention, Atlanta, Georgia 30329, USA.
authors.forename: Xiyan
authors.initials: X
authors.lastname: Xu
authors.affiliation: Department of Microbiology and Immunology, Rega Institute, KU Leuven - University of Leuven, 3000 Leuven, Belgium.
authors.forename: Philippe
authors.initials: P
authors.lastname: Lemey
authors.affiliation: Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, UK.
authors.forename: Colin A
authors.initials: CA
authors.lastname: Russell
mesh_terms: D000367:Age Factors; D000940:Antigenic Variation; D014943:Global Health; D006801:Humans; D009980:Influenza A virus / Q000145:classification / Q000235:genetics*; D009981:Influenza B virus / Q000145:classification / Q000235:genetics*; D007251:Influenza, Human / Q000453:epidemiology* / Q000821:virology*; D010802:Phylogeny; D058974:Phylogeography; D012621:Seasons