eLife (Sep 2024)
Antigenic drift and subtype interference shape A(H3N2) epidemic dynamics in the United States
- Amanda C Perofsky,
- John Huddleston,
- Chelsea L Hansen,
- John R Barnes,
- Thomas Rowe,
- Xiyan Xu,
- Rebecca Kondor,
- David E Wentworth,
- Nicola Lewis,
- Lynne Whittaker,
- Burcu Ermetal,
- Ruth Harvey,
- Monica Galiano,
- Rodney Stuart Daniels,
- John W McCauley,
- Seiichiro Fujisaki,
- Kazuya Nakamura,
- Noriko Kishida,
- Shinji Watanabe,
- Hideki Hasegawa,
- Sheena G Sullivan,
- Ian G Barr,
- Kanta Subbarao,
- Florian Krammer,
- Trevor Bedford,
- Cécile Viboud
Affiliations
- Amanda C Perofsky
- ORCiD
- Fogarty International Center, National Institutes of Health, Bethesda, United States; Brotman Baty Institute for Precision Medicine, University of Washington, Seattle, United States
- John Huddleston
- ORCiD
- Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, United States
- Chelsea L Hansen
- ORCiD
- Fogarty International Center, National Institutes of Health, Bethesda, United States; Brotman Baty Institute for Precision Medicine, University of Washington, Seattle, United States
- John R Barnes
- Virology Surveillance and Diagnosis Branch, Influenza Division, National Center for Immunization and Respiratory Diseases (NCIRD), Centers for Disease Control and Prevention (CDC), Atlanta, United States
- Thomas Rowe
- Virology Surveillance and Diagnosis Branch, Influenza Division, National Center for Immunization and Respiratory Diseases (NCIRD), Centers for Disease Control and Prevention (CDC), Atlanta, United States
- Xiyan Xu
- Virology Surveillance and Diagnosis Branch, Influenza Division, National Center for Immunization and Respiratory Diseases (NCIRD), Centers for Disease Control and Prevention (CDC), Atlanta, United States
- Rebecca Kondor
- ORCiD
- Virology Surveillance and Diagnosis Branch, Influenza Division, National Center for Immunization and Respiratory Diseases (NCIRD), Centers for Disease Control and Prevention (CDC), Atlanta, United States
- David E Wentworth
- ORCiD
- Virology Surveillance and Diagnosis Branch, Influenza Division, National Center for Immunization and Respiratory Diseases (NCIRD), Centers for Disease Control and Prevention (CDC), Atlanta, United States
- Nicola Lewis
- WHO Collaborating Centre for Reference and Research on Influenza, Crick Worldwide Influenza Centre, The Francis Crick Institute, London, United Kingdom
- Lynne Whittaker
- WHO Collaborating Centre for Reference and Research on Influenza, Crick Worldwide Influenza Centre, The Francis Crick Institute, London, United Kingdom
- Burcu Ermetal
- WHO Collaborating Centre for Reference and Research on Influenza, Crick Worldwide Influenza Centre, The Francis Crick Institute, London, United Kingdom
- Ruth Harvey
- WHO Collaborating Centre for Reference and Research on Influenza, Crick Worldwide Influenza Centre, The Francis Crick Institute, London, United Kingdom
- Monica Galiano
- WHO Collaborating Centre for Reference and Research on Influenza, Crick Worldwide Influenza Centre, The Francis Crick Institute, London, United Kingdom
- Rodney Stuart Daniels
- ORCiD
- WHO Collaborating Centre for Reference and Research on Influenza, Crick Worldwide Influenza Centre, The Francis Crick Institute, London, United Kingdom
- John W McCauley
- ORCiD
- WHO Collaborating Centre for Reference and Research on Influenza, Crick Worldwide Influenza Centre, The Francis Crick Institute, London, United Kingdom
- Seiichiro Fujisaki
- Influenza Virus Research Center, National Institute of Infectious Diseases, Tokyo, Japan
- Kazuya Nakamura
- Influenza Virus Research Center, National Institute of Infectious Diseases, Tokyo, Japan
- Noriko Kishida
- Influenza Virus Research Center, National Institute of Infectious Diseases, Tokyo, Japan
- Shinji Watanabe
- Influenza Virus Research Center, National Institute of Infectious Diseases, Tokyo, Japan
- Hideki Hasegawa
- Influenza Virus Research Center, National Institute of Infectious Diseases, Tokyo, Japan
- Sheena G Sullivan
- WHO Collaborating Centre for Reference and Research on Influenza, The Peter Doherty Institute for Infection and Immunity, Department of Microbiology and Immunology, The University of Melbourne, The Peter Doherty Institute for Infection and Immunity, Melbourne, Australia
- Ian G Barr
- WHO Collaborating Centre for Reference and Research on Influenza, The Peter Doherty Institute for Infection and Immunity, Department of Microbiology and Immunology, The University of Melbourne, The Peter Doherty Institute for Infection and Immunity, Melbourne, Australia
- Kanta Subbarao
- ORCiD
- WHO Collaborating Centre for Reference and Research on Influenza, The Peter Doherty Institute for Infection and Immunity, Department of Microbiology and Immunology, The University of Melbourne, The Peter Doherty Institute for Infection and Immunity, Melbourne, Australia
- Florian Krammer
- Center for Vaccine Research and Pandemic Preparedness (C-VaRPP), Icahn School of Medicine at Mount Sinai, New York, United States; Department of Pathology, Molecular and Cell-Based Medicine, Icahn School of Medicine at Mount Sinai, New York, United States
- Trevor Bedford
- ORCiD
- Brotman Baty Institute for Precision Medicine, University of Washington, Seattle, United States; Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, United States; Department of Genome Sciences, University of Washington, Seattle, United States; Howard Hughes Medical Institute, Seattle, United States
- Cécile Viboud
- ORCiD
- Fogarty International Center, National Institutes of Health, Bethesda, United States
- DOI
- https://doi.org/10.7554/eLife.91849
- Journal volume & issue
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Vol. 13
Abstract
Influenza viruses continually evolve new antigenic variants, through mutations in epitopes of their major surface proteins, hemagglutinin (HA) and neuraminidase (NA). Antigenic drift potentiates the reinfection of previously infected individuals, but the contribution of this process to variability in annual epidemics is not well understood. Here, we link influenza A(H3N2) virus evolution to regional epidemic dynamics in the United States during 1997—2019. We integrate phenotypic measures of HA antigenic drift and sequence-based measures of HA and NA fitness to infer antigenic and genetic distances between viruses circulating in successive seasons. We estimate the magnitude, severity, timing, transmission rate, age-specific patterns, and subtype dominance of each regional outbreak and find that genetic distance based on broad sets of epitope sites is the strongest evolutionary predictor of A(H3N2) virus epidemiology. Increased HA and NA epitope distance between seasons correlates with larger, more intense epidemics, higher transmission, greater A(H3N2) subtype dominance, and a greater proportion of cases in adults relative to children, consistent with increased population susceptibility. Based on random forest models, A(H1N1) incidence impacts A(H3N2) epidemics to a greater extent than viral evolution, suggesting that subtype interference is a major driver of influenza A virus infection ynamics, presumably via heterosubtypic cross-immunity.
Keywords
