Characterization of contemporary 2010.1 H3N2 swine influenza A viruses circulating in United States pigs

Authors: POWELL, JOSHUA - Orise Fellow; ABENTE, EUGENIO - US Department Of Agriculture (USDA); CHANG, JENNIFER - Orise Fellow; SOUZA, CARINE - Orise Fellow; RAJAO, DANIELA - Orise Fellow; Anderson, Tavis; ZELLER, MICHAEL - Iowa State University; GAUGER, PHIL - Iowa State University; LEWIS, NICOLA - Royal Veterinary College; Baker, Amy

Submitted to: Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/17/2020
Publication Date: 1/15/2021
Citation: Powell, J.D., Abente, E.J., Chang, J., Souza, C.K., Rajao, D.S., Anderson, T.K., Zeller, M.A., Gauger, P.C., Lewis, N.S., Vincent, A.L. 2021. Characterization of contemporary 2010.1 H3N2 swine influenza A viruses circulating in United States pigs. Virology. 553:94-101. https://doi.org/10.1016/j.virol.2020.11.006.
DOI: https://doi.org/10.1016/j.virol.2020.11.006

Interpretive Summary: Influenza A virus (IAV) is an important pathogen in birds, humans, pigs and other mammals. Spread of IAV from humans to pigs plays an important role in the diversity of IAV found in pig populations, and the diversity of IAV in pigs complicates control by swine vaccines. During the 2010-11 human influenza season, a human H3N2 IAV infected pigs in the U.S., a portion of its genome, the hemagglutinin gene, was maintained in swine, and these viruses continue to be frequently detected in swine herds. We sought to investigate how these H3N2 have changed over time by assessing recognition by the swine antibody response and by infection properties in pigs. This understanding will indicate the risk to swine populations and aid in improving influenza vaccines used in the swine industry. This swine H3N2 IAV also previously infected people at multiple agricultural fairs and therefore is a public health concern. We showed in this report that these swine H3N2 IAV have evolved in recent years to acquire genetic changes related to evading antibody immunity, and each of the genotypes we tested were fully capable of infecting pigs, causing disease and spreading among pigs. These contemporary swine H3N2 viruses should be considered for inclusion in swine influenza vaccines and as a potential risk to humans.

Technical Abstract: In 2012, swine influenza A surveillance detected a novel reassorted influenza A virus (IAV) strain containing human-seasonal hemagglutinin (HA) and neuraminidase (NA) genes with internal genes derived from H1N1pdm09 IAV. Subsequently, these viruses reassorted, maintaining the human-origin H3 and H1N1pdm09 M genes, but replacing all other segments, resulting in a new lineage of viruses that became the most frequently detected H3 clade in US swine (2010.1 HA clade). Here, we assessed the antigenic phenotype, virulence, and transmission characteristics of this virus lineage across 6 years of sustained circulation following its introduction to swine. Relative to 2010.1 viruses from 2012 and 2014, more recent 2010.1 contemporary strains from 2015-2017 resulted in equivalent macroscopic lung lesions and transmission in pigs. A single mutation at amino acid residue 145 within the previously defined HA antigenic motif was associated with a change of antigenic phenotype, potentially impairing vaccine efficacy. Our data demonstrate that human to swine transmission, followed by evolution and antigenic drift of 2010.1 H3, resulted in a sustained dominant monophyletic H3 clade in swine. 2010.1 viruses circulating in swine are now significantly different from pre-2012 H3N2 in swine as well as antigenic drift from human-seasonal H3N2 viruses.