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Title: Reassortment between swine H3N2 and 2009 pandemic H1N1 in the United States resulted in influenza A viruses with diverse genetic constellations with variable virulence in pigs

Author
item RAJAO, DANIELA - Non ARS Employee
item WALIA, RASNA - Orise Fellow
item Campbell, Brian
item GAUGER, PHILLIP - Iowa State University
item JANAS-MARTINDALE, ALICIA - Animal And Plant Health Inspection Service (APHIS)
item KILLIAN, MARY LEA - Animal And Plant Health Inspection Service (APHIS)
item Baker, Amy

Submitted to: Journal of Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/1/2016
Publication Date: 1/31/2017
Citation: Rajao, D.S., Walia, R.R., Campbell, B., Gauger, P.C., Janas-Martindale, A., Killian, M.L., Vincent, A.L. 2017. Reassortment between swine H3N2 and 2009 pandemic H1N1 in the United States resulted in influenza A viruses with diverse genetic constellations with variable virulence in pigs. Journal of Virology. 91:e01763-16. doi.org/10.1128/JVI.01763-16.

Interpretive Summary: A pandemic H1N1 influenza virus (H1N1pdm09) spread through humans globally in 2009 and was quickly introduced into swine herds. People continue to spread the H1N1pdm09 to pigs, allowing it to exchange genetic material in a process called reassortment in different combinations with influenza viruses that normally circulate in swine, including the H3N2 subtype. In this study, we examined the genetic makeup of H3N2 influenza viruses that were detected from 2009-2016 in pigs in the U.S. and identified 44 different gene combinations (also called genotypes) generated by reassortment between H1N1pdm09 from humans and the H3N2 from swine. We compared the properties of six of these genotypes in pigs, which resulted in different degrees of disease. These results highlight the vast genetic diversity of H3N2 influenza viruses circulating in U.S. swine after 2009, making it difficult to control the disease by the swine industry. Because some of these genetic combinations may contain genetic material from the H1N1pdm09 that is highly adapted to humans, some of these swine viruses may have increased potential risk for human infection.

Technical Abstract: Repeated spillovers of the H1N1 pandemic virus (H1N1pdm09) from humans to pigs resulted in substantial evolution of swine influenza viruses, contributing to the genetic and antigenic diversity of influenza A virus (IAV) currently circulating in swine. The reassortment with endemic swine viruses and maintenance of some of the H1N1pdm09 internal genes resulted in the circulation of different genomic constellations in pigs. Here, we performed a whole genome phylogenetic analysis of 496 IAV circulating in swine from 2009 to 2016 in the U.S. We identified 44 different genotypes, with the most common genotype (32.33%) containing a cluster IV-A HA gene, a 2002-lineage NA gene, an M-pdm09 gene, and remaining gene segments of triple reassortant internal gene (TRIG) origin. To understand how different genetic constellations may relate to viral fitness, we compared the pathogenesis and transmission in pigs of six representative genotypes. Although all six genotypes efficiently infected pigs, they resulted in different degrees of pathology and viral shedding. These results highlight the vast H3N2 genetic diversity circulating in U.S. swine after 2009. This diversity has important implications to the control of this disease by the swine industry, as well as a potential risk for public health if swine-adapted viruses with H1N1pdm09 genes have an increased risk to humans.