Introduction, evolution, and dissemination of influenza A viruses in exhibition swine in the United States during 2009 to 2013

Martha I. Nelson, Karla M. Stucker, Seth A. Schobel, Nídia S. Trovão, Suman R. Das, Vivien G. Dugan, Sarah W. Nelson, Srinand Sreevatsan, Mary L. Killian, Jacqueline M. Nolting, David E. Wentworth, Andrew S. Bowman

Research output: Contribution to journalArticlepeer-review

11 Scopus citations

Abstract

The swine-human interface created at agricultural fairs, along with the generation of and maintenance of influenza A virus diversity in exhibition swine, presents an ongoing threat to public health. Nucleotide sequences of influenza A virus isolates collected from exhibition swine in Ohio (n=262) and Indiana (n=103) during 2009 to 2013 were used to investigate viral evolution and movement within this niche sector of the swine industry. Phylogenetic and Bayesian analyses were employed to identify introductions of influenza A virus to exhibition swine and study viral population dynamics. In 2013 alone, we identified 10 independent introductions of influenza A virus into Ohio and/or Indiana exhibition swine. Frequently, viruses from the same introduction were identified at multiple fairs within the region, providing evidence of rapid and widespread viral movement within the exhibition swine populations of the two states. While pigs moving from fair to fair to fair is possible in some locations, the concurrent detection of nearly identical strains at several fairs indicates that a common viral source was more likely. Importantly, we detected an association between the high number of human variant H3N2 (H3N2v) virus infections in 2012 and the widespread circulation of influenza A viruses of the same genotype in exhibition swine in Ohio fairs sampled that year. The extent of viral diversity observed in exhibition swine and the rapidity with which it disseminated across long distances indicate that novel strains of influenza A virus will continue to emerge and spread within exhibition swine populations, presenting an ongoing threat to humans.

Original languageEnglish (US)
Pages (from-to)10963-10971
Number of pages9
JournalJournal of virology
Volume90
Issue number23
DOIs
StatePublished - 2016

Bibliographical note

Funding Information:
We thank all our participating agricultural fairs and the field staff who tirelessly collected these samples. We also thank Jody Edwards for her laboratory expertise and technical abilities and the skilled staff at all sequencing centers for their meticulous efforts to provide the high-quality genome sequences used for these analyses. Additional thanks go to Allison Schwam for assistance with data set curation and genotype proportion analysis. The opinions expressed in this article are the authors' opinions and do not reflect the views of the Department of Agriculture, the Department of Health and Human Services, or the U.S. government. This work was funded with federal funds from the Centers of Excellence for Influenza Research and Surveillance (CEIRS), the National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), and the Department of Health and Human Services (HHS) under contracts HHSN272201400006C, HHSN272201400008C, and HHSN266200700007C. The sequencing work was funded with federal funds for the Genomic Sequencing Centers for Infectious Diseases (GSCID) by the NIAID, NIH, HHS, under contract HHSN272200900007C, as well as with the Genomic Centers for Infectious Diseases (GCID) U19 program (U19-AI-110819) by the NIAID, NIH, HHS. This work was supported in part by the Multinational Influenza Seasonal Mortality Study (MISMS), an ongoing international collaborative effort to understand influenza epidemiology and evolution, led by the Fogarty International Center, NIH. Additional support was provided the USDA/APHIS NVSL. Any mention of trade names or commercial products is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. We declare that we have no competing interests. This work, including the efforts of Sarah W. Nelson, Jacqueline M. Nolting, and Andrew S. Bowman, was funded by HHS | National Institutes of Health (NIH) (HHSN272201400006C). This work, including the efforts of Martha I. Nelson, was funded by HHS | National Institutes of Health (NIH) (HHSN272201400008C). This work, including the efforts of Sarah W. Nelson, Srinand Sreevatsan, Jacqueline M. Nolting, and Andrew S. Bowman, was funded by HHS | National Institutes of Health (NIH) (HHSN266200700007C). This work, including the efforts of Karla M. Stucker, Seth A. Schobel, Suman R. Das, Vivien G. Dugan, and David E. Wentworth, was funded by HHS | National Institutes of Health (NIH) (HHSN272200900007C). This work, including the efforts of Suman R. Das and David E. Wentworth, was funded by HHS | National Institutes of Health (NIH) (U19-AI-110819).

Publisher Copyright:
© 2016, American Society for Microbiology. All Rights Reserved.

Copyright:
Copyright 2017 Elsevier B.V., All rights reserved.

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