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Genetic Diversity and Evolution

A Heterogeneous Swine Show Circuit Drives Zoonotic Transmission of Influenza A Viruses in the United States

Martha I. Nelson, Amanda Perofsky, Dillon S. McBride, Benjamin L. Rambo-Martin, Malania M. Wilson, John R. Barnes, Harm van Bakel, Zenab Khan, Jayeeta Dutta, Jacqueline M. Nolting, Andrew S. Bowman
Colin R. Parrish, Editor
Martha I. Nelson
aFogarty International Center, National Institutes of Health, Bethesda, Maryland, USA
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Amanda Perofsky
aFogarty International Center, National Institutes of Health, Bethesda, Maryland, USA
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Dillon S. McBride
bDepartment of Veterinary Preventive Medicine, Ohio State University, Columbus, Ohio, USA
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Benjamin L. Rambo-Martin
cInfluenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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  • ORCID record for Benjamin L. Rambo-Martin
Malania M. Wilson
cInfluenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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John R. Barnes
cInfluenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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Harm van Bakel
dIcahn School of Medicine at Mount Sinai, New York, New York, USA
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Zenab Khan
dIcahn School of Medicine at Mount Sinai, New York, New York, USA
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Jayeeta Dutta
dIcahn School of Medicine at Mount Sinai, New York, New York, USA
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Jacqueline M. Nolting
bDepartment of Veterinary Preventive Medicine, Ohio State University, Columbus, Ohio, USA
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Andrew S. Bowman
bDepartment of Veterinary Preventive Medicine, Ohio State University, Columbus, Ohio, USA
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Colin R. Parrish
Cornell University
Roles: Editor
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DOI: 10.1128/JVI.01453-20
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ABSTRACT

Influenza pandemics are associated with severe morbidity, mortality, and social and economic disruption. Every summer in the United States, youths attending agricultural fairs are exposed to genetically diverse influenza A viruses (IAVs) circulating in exhibition swine, resulting in over 450 lab-confirmed zoonotic infections since 2010. Exhibition swine represent a small, defined population (∼1.5% of the U.S. herd), presenting a realistic opportunity to mitigate a pandemic threat by reducing IAV transmission in the animals themselves. Through intensive surveillance and genetic sequencing of IAVs in exhibition swine in six U.S. states in 2018 (n = 212), we characterized how a heterogeneous circuit of swine shows, comprising fairs with different sizes and geographic coverage, facilitates IAV transmission among exhibition swine and into humans. Specifically, we identified the role of an early-season national show in the propagation and spatial dissemination of a specific virus (H1δ-2) that becomes dominant among exhibition swine and is associated with the majority of zoonotic infections in 2018. These findings suggest that a highly targeted mitigation strategy, such as postponing swine shows for 1 to 2 weeks following the early-season national show, could potentially reduce IAV transmission in exhibition swine and spillover into humans, and this merits further study.

IMPORTANCE The varying influenza A virus (IAV) exposure and infection status of individual swine facilitates introduction, transmission, and dissemination of diverse IAVs. Since agricultural fairs bring people into intimate contact with swine, they provide a unique interface for zoonotic transmission of IAV. Understanding the dynamics of IAV transmission through exhibition swine is critical to mitigating the high incidence of variant IAV cases reported in association with agricultural fairs. We used genomic sequences from our exhibition swine surveillance to characterize the hemagglutinin and full genotypic diversity of IAV at early-season shows and the subsequent dissemination through later-season agricultural fairs. We were able to identify a critical time point with important implications for downstream IAV and zoonotic transmission. With improved understanding of evolutionary origins of zoonotic IAV, we can inform public health mitigation strategies to ultimately reduce zoonotic IAV transmission and risk of pandemic IAV emergence.

FOOTNOTES

    • Received 17 July 2020.
    • Accepted 22 September 2020.
    • Accepted manuscript posted online 30 September 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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A Heterogeneous Swine Show Circuit Drives Zoonotic Transmission of Influenza A Viruses in the United States
Martha I. Nelson, Amanda Perofsky, Dillon S. McBride, Benjamin L. Rambo-Martin, Malania M. Wilson, John R. Barnes, Harm van Bakel, Zenab Khan, Jayeeta Dutta, Jacqueline M. Nolting, Andrew S. Bowman
Journal of Virology Nov 2020, 94 (24) e01453-20; DOI: 10.1128/JVI.01453-20

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A Heterogeneous Swine Show Circuit Drives Zoonotic Transmission of Influenza A Viruses in the United States
Martha I. Nelson, Amanda Perofsky, Dillon S. McBride, Benjamin L. Rambo-Martin, Malania M. Wilson, John R. Barnes, Harm van Bakel, Zenab Khan, Jayeeta Dutta, Jacqueline M. Nolting, Andrew S. Bowman
Journal of Virology Nov 2020, 94 (24) e01453-20; DOI: 10.1128/JVI.01453-20
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KEYWORDS

genomic epidemiology
influenza A virus
public health
swine
zoonoses

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