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Title: Characterization of co-circulating swine influenza A viruses in North America and the identification of a novel H1 genetic clade with antigenic significance

Author
item Anderson, Tavis
item Campbell, Brian
item NELSON, MARTHA - Fogarty International Center
item LEWIS, NICOLA - University Of Cambridge
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: Virus Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/10/2015
Publication Date: 4/1/2015
Citation: Anderson, T.K., Campbell, B.A., Nelson, M.I., Lewis, N.S., Janas-Martindale, A., Killian, M., Vincent, A.L. 2015. Characterization of co-circulating swine influenza A viruses in North America and the identification of a novel H1 genetic clade with antigenic significance. Virus Research. 201:24–31.

Interpretive Summary: Understanding the dynamics of influenza A viruses (IAV) in the swine population is critical to understanding the evolution of influenza viruses overall. IAV genetic makeup continually changes, and monitoring the patterns of swine IAV genetic change is needed to identify possible emerging influenza threats. This study compared the swine IAV patterns from 2013-2014 with the baseline data from 2009-2102. In doing so, we discovered a previously uncharacterized distinct genetic and antigenic group of viruses that circulated for a period of years at low levels, disappeared, and then re-emerged in 2010. The long-term circulation of these viruses suggests that minor populations of viruses may be underreported in the national dataset. The identification of these viruses demonstrates the importance of a robust USDA surveillance system for IAV in swine to inform control measures taken against IAV. This paper aids in improving agricultural production and pandemic preparedness by allowing for the identification of important changes in virus evolution and providing a benchmark from which to measure success of intervention strategies. These interventions include timely vaccine and diagnostic updates for use in swine and humans, as well as factors to prevent infection and transmission, such as changes in production practices or farm management.

Technical Abstract: Multiple genetically and antigenically distinct hemagglutinin genes of the H1 and H3 influenza A virus (IAV) subtypes co-circulate in North American swine. This diversity has evolved by repeated transmission of IAVs from humans to swine and subsequent antigenic drift in swine. To understand the evolutionary dynamics of these diverse HA lineages in North American swine, we undertook a phylogenetic analysis of 1576 H1 and 607 H3 HA gene segments, as well as 834 N1 and 1293 N2 NA gene segments, and 2126 M gene segments. These data revealed yearly co-circulation of H1N1, H1N2, and H3N2 viruses, with three HA clades representing the majority of the HA sequences: of the H1 viruses, 42% were classified as H1delta1 and 40.6% were classified as H1gamma; and of the H3 viruses 53% were classified as cluster IV-A H3N2. We detected a genetically distinct minor clade consisting of 37 H1 viruses, which we classified as H1gamma-2. This clade has circulated in swine since about 1995 and has been detected in swine as recently as 2013. Importantly, hemagglutination inhibition (HI) assays demonstrated that representatives of this clade of viruses are antigenically distinct, and as many as 7 antigenic units from other H1gamma viruses, and therefore vaccines against the contemporary H1gamma viruses are not likely to cross-protect against gamma-2 viruses. The long-term circulation of these gamma-2 viruses suggests that minor populations of viruses may be underreported in the national dataset given the long branch lengths and gaps in detections. The identification of these gamma-2 viruses demonstrates the importance of antigenic drift in the diversification and emergence of new antigenic variants in swine, which complicates vaccine design, and the need for robust surveillance to capture the full diversity IAVs in swine in the USA.