Phylogenetic Analyses of North American Exhibition Swine Influenza A Viruses from 2009 to 2013

Allison Schwam, Karla M. Stucker, Seth A. Schobel, Xudong Lin, Rebecca A. Halpin, Nadia Fedorova, Timothy B. Stockwell, Richard D. Slemons, Suman R. Das, Martha Nelson, Andrew S. Bowman, David E. Wentworth

We studied the evolution of swine influenza A viruses (IAVs) to gain a better understanding of the movement of IAVs among commercial and exhibition swine, as well as spillover into human hosts. IAV is a segmented, negative-sense RNA virus that is classified by the viral surface proteins hemagglutinin (HA or H) and neuraminidase (NA or N).  Of the three species of influenza viruses (A, B and C), IAV is the most virulent human pathogen and causes the majority of outbreaks of severe illness.  We analyzed North American swine IAVs circulating since the emergence of the human 2009 H1N1pdm in commercial and exhibition swine, as well as human cases of variant swine-origin influenza infections in the US.  Specific fair locations in Ohio where exhibition swine were held were sampled for IAV. The fairs provide opportunities for increased swine and human interactions, likely promoting the exchange of IAVs between swine and humans. Pigs are susceptible to infection by human seasonal IAVs (H1N1, H3N2) and maintain their own lineages of the same IAV subtypes. Viral reassortment occurs when two viruses infect the same cell and exchange genetic segments, providing one mechanism for viral evolution. Pigs are generally considered to be “mixing vessels” for IAVs because they are a common source for reassorted IAVs that can spillover into human hosts. However, it is important to recognize that IAVs are transmitted in both directions: swine to human and human to swine. By sequencing coding-complete genomes of Ohio exhibition swine IAVs and using phylogenetic analysis techniques, we were able to infer the evolutionary histories of these IAVs and place them in the context of related commercial swine and variant swine-origin human IAVs. These analyses show that the North American commercial and exhibition swine IAV genetic make-up has shifted over time, with the H1N1pdm matrix segment becoming more prevalent in all swine IAVs over time, suggesting that human-swine interactions (e.g., at fairs) have resulted in the cross-species transmission of IAVs that contributes to novel IAV reassortment and evolution.