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Pandemic Paradox: Early Life H2N2 Pandemic Influenza Infection Enhanced Susceptibility to Death during the 2009 H1N1 Pandemic.
mBio. 2018 01 16; 9(1)MBIO

Abstract

Recent outbreaks of H5, H7, and H9 influenza A viruses in humans have served as a vivid reminder of the potentially devastating effects that a novel pandemic could exert on the modern world. Those who have survived infections with influenza viruses in the past have been protected from subsequent antigenically similar pandemics through adaptive immunity. For example, during the 2009 H1N1 "swine flu" pandemic, those exposed to H1N1 viruses that circulated between 1918 and the 1940s were at a decreased risk for mortality as a result of their previous immunity. It is also generally thought that past exposures to antigenically dissimilar strains of influenza virus may also be beneficial due to cross-reactive cellular immunity. However, cohorts born during prior heterosubtypic pandemics have previously experienced elevated risk of death relative to surrounding cohorts of the same population. Indeed, individuals born during the 1890 H3Nx pandemic experienced the highest levels of excess mortality during the 1918 "Spanish flu." Applying Serfling models to monthly mortality and influenza circulation data between October 1997 and July 2014 in the United States and Mexico, we show corresponding peaks in excess mortality during the 2009 H1N1 "swine flu" pandemic and during the resurgent 2013-2014 H1N1 outbreak for those born at the time of the 1957 H2N2 "Asian flu" pandemic. We suggest that the phenomenon observed in 1918 is not unique and points to exposure to pandemic influenza early in life as a risk factor for mortality during subsequent heterosubtypic pandemics.IMPORTANCE The relatively low mortality experienced by older individuals during the 2009 H1N1 influenza virus pandemic has been well documented. However, reported situations in which previous influenza virus exposures have enhanced susceptibility are rare and poorly understood. One such instance occurred in 1918-when those born during the heterosubtypic 1890 H3Nx influenza virus pandemic experienced the highest levels of excess mortality. Here, we demonstrate that this phenomenon was not unique to the 1918 H1N1 pandemic but that it also occurred during the contemporary 2009 H1N1 pandemic and 2013-2014 H1N1-dominated season for those born during the heterosubtypic 1957 H2N2 "Asian flu" pandemic. These data highlight the heretofore underappreciated phenomenon that, in certain instances, prior exposure to pandemic influenza virus strains can enhance susceptibility during subsequent pandemics. These results have important implications for pandemic risk assessment and should inform laboratory studies aimed at uncovering the mechanism responsible for this effect.

Authors+Show Affiliations

Department of Demography, Université de Montréal, Montréal, Canada. Université de Montréal Public Health Research Institute (IRSPUM), Montréal, Canada.Department of Demography, Université de Montréal, Montréal, Canada.Statistics Canada, Ottawa, Canada.Department of Demography, Université de Montréal, Montréal, Canada.Department of Demography, Université de Montréal, Montréal, Canada.Department of Demography, Université de Montréal, Montréal, Canada.Department of Mathematics and Statistics, McMaster University, Hamilton, Canada. Michael G. DeGroote Institute for Infectious Diseases Research, McMaster University, Hamilton, Canada.Department of Anthropology, McMaster University, Hamilton, Canada.Department of Economics and Finance, Department of History, University of Guelph, Guelph, Canada.Los Angeles Biomedical Research Institute at Harbor, UCLA Medical Center, Los Angeles, California, USA.Michael G. DeGroote Institute for Infectious Diseases Research, McMaster University, Hamilton, Canada mmiller@mcmaster.ca. Department of Biochemistry and Biomedical Sciences, McMaster Immunology Research Centre, McMaster University, Hamilton, Canada.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

29339427

Citation

Gagnon, Alain, et al. "Pandemic Paradox: Early Life H2N2 Pandemic Influenza Infection Enhanced Susceptibility to Death During the 2009 H1N1 Pandemic." MBio, vol. 9, no. 1, 2018.
Gagnon A, Acosta E, Hallman S, et al. Pandemic Paradox: Early Life H2N2 Pandemic Influenza Infection Enhanced Susceptibility to Death during the 2009 H1N1 Pandemic. mBio. 2018;9(1).
Gagnon, A., Acosta, E., Hallman, S., Bourbeau, R., Dillon, L. Y., Ouellette, N., Earn, D. J. D., Herring, D. A., Inwood, K., Madrenas, J., & Miller, M. S. (2018). Pandemic Paradox: Early Life H2N2 Pandemic Influenza Infection Enhanced Susceptibility to Death during the 2009 H1N1 Pandemic. MBio, 9(1). https://doi.org/10.1128/mBio.02091-17
Gagnon A, et al. Pandemic Paradox: Early Life H2N2 Pandemic Influenza Infection Enhanced Susceptibility to Death During the 2009 H1N1 Pandemic. mBio. 2018 01 16;9(1) PubMed PMID: 29339427.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Pandemic Paradox: Early Life H2N2 Pandemic Influenza Infection Enhanced Susceptibility to Death during the 2009 H1N1 Pandemic. AU - Gagnon,Alain, AU - Acosta,Enrique, AU - Hallman,Stacey, AU - Bourbeau,Robert, AU - Dillon,Lisa Y, AU - Ouellette,Nadine, AU - Earn,David J D, AU - Herring,D Ann, AU - Inwood,Kris, AU - Madrenas,Joaquin, AU - Miller,Matthew S, Y1 - 2018/01/16/ PY - 2018/1/18/entrez PY - 2018/1/18/pubmed PY - 2018/12/12/medline KW - influenza virus KW - mortality KW - pandemics KW - susceptibility JF - mBio JO - mBio VL - 9 IS - 1 N2 - Recent outbreaks of H5, H7, and H9 influenza A viruses in humans have served as a vivid reminder of the potentially devastating effects that a novel pandemic could exert on the modern world. Those who have survived infections with influenza viruses in the past have been protected from subsequent antigenically similar pandemics through adaptive immunity. For example, during the 2009 H1N1 "swine flu" pandemic, those exposed to H1N1 viruses that circulated between 1918 and the 1940s were at a decreased risk for mortality as a result of their previous immunity. It is also generally thought that past exposures to antigenically dissimilar strains of influenza virus may also be beneficial due to cross-reactive cellular immunity. However, cohorts born during prior heterosubtypic pandemics have previously experienced elevated risk of death relative to surrounding cohorts of the same population. Indeed, individuals born during the 1890 H3Nx pandemic experienced the highest levels of excess mortality during the 1918 "Spanish flu." Applying Serfling models to monthly mortality and influenza circulation data between October 1997 and July 2014 in the United States and Mexico, we show corresponding peaks in excess mortality during the 2009 H1N1 "swine flu" pandemic and during the resurgent 2013-2014 H1N1 outbreak for those born at the time of the 1957 H2N2 "Asian flu" pandemic. We suggest that the phenomenon observed in 1918 is not unique and points to exposure to pandemic influenza early in life as a risk factor for mortality during subsequent heterosubtypic pandemics.IMPORTANCE The relatively low mortality experienced by older individuals during the 2009 H1N1 influenza virus pandemic has been well documented. However, reported situations in which previous influenza virus exposures have enhanced susceptibility are rare and poorly understood. One such instance occurred in 1918-when those born during the heterosubtypic 1890 H3Nx influenza virus pandemic experienced the highest levels of excess mortality. Here, we demonstrate that this phenomenon was not unique to the 1918 H1N1 pandemic but that it also occurred during the contemporary 2009 H1N1 pandemic and 2013-2014 H1N1-dominated season for those born during the heterosubtypic 1957 H2N2 "Asian flu" pandemic. These data highlight the heretofore underappreciated phenomenon that, in certain instances, prior exposure to pandemic influenza virus strains can enhance susceptibility during subsequent pandemics. These results have important implications for pandemic risk assessment and should inform laboratory studies aimed at uncovering the mechanism responsible for this effect. SN - 2150-7511 UR - https://www.unboundmedicine.com/medline/citation/29339427/Pandemic_Paradox:_Early_Life_H2N2_Pandemic_Influenza_Infection_Enhanced_Susceptibility_to_Death_during_the_2009_H1N1_Pandemic_ L2 - http://mbio.asm.org/cgi/pmidlookup?view=long&pmid=29339427 DB - PRIME DP - Unbound Medicine ER -