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Research Project: Intervention Strategies to Control Influenza A Virus Infection in Swine

Location: Virus and Prion Research

Title: Characterization of a 2016-2017 human-seasonal H3 influenza A virus spillover now endemic to U.S. swine

Author
item SHARMA, ADITI - Iowa State University
item ZELLER, MICHAEL - Iowa State University
item SOUZA, CARINE - Orise Fellow
item Anderson, Tavis
item Vincent, Amy
item HARMON, KAREN - Iowa State University
item LI, GANWU - Iowa State University
item ZHANG, JIANQIANG - Iowa State University
item GAUGER, PHILLIP - Iowa State University

Submitted to: mSphere
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/3/2022
Publication Date: 1/12/2022
Citation: Sharma, A., Zeller, M.A., Souza, C.K., Anderson, T.K., Baker, A.L., Harmon, K., Li, G., Zhang, J., Gauger, P.C. 2022. Characterization of a 2016-2017 human-seasonal H3 influenza A virus spillover now endemic to U.S. swine. mSphere. 7(1). Article e00809-21. https://doi.org/10.1128/msphere.00809-21.
DOI: https://doi.org/10.1128/msphere.00809-21

Interpretive Summary: The H3.2010.2 is a new phylogenetic clade of H3N2 circulating in swine that became established after the spillover of a human seasonal H3N2 from the 2016-17 influenza season. The novel H3.2010.2 transmitted and adapted to the swine host and demonstrated reassortment with internal genes from endemic strains, but maintained human-like HA and NA. It is genetically and antigenically distinct from the H3.2010.1 H3N2 introduced earlier in the 2010 decade. Human-seasonal IAV spillovers into swine become established in the population through adaptation and sustained transmission and contribute to the genetic and antigenic diversity of IAV circulating in swine. Continued IAV surveillance is necessary to detect emergence of novel strains in swine and assist with vaccine antigen selection to improve the ability to prevent respiratory disease in swine as well as the risk of zoonotic transmission.

Technical Abstract: In 2017, the Iowa State University Veterinary Diagnostic Laboratory detected a reverse-zoonotic transmission of a human seasonal H3 influenza A virus into swine (IAV-S) in Oklahoma. Pairwise comparison between the first H3.2010.2 hemagglutinin (HA) sequences detected in swine and the most similar 2016-2017 human seasonal H3 revealed 99.9% nucleotide identity. To understand the origin of H3.2010.2 IAV-S, 45 HA and 27 neuraminidase (NA) sequences from 2017-2020 as well as 11 whole genome sequences (WGS) were genetically characterized. Time to most recent common human ancestor was estimated between August-September 2016. The N2 NA was of human origin in all but one strain from diagnostic submissions with NA sequences, and the internal gene segments from WGS consisted of matrix genes originating from the 2009 pandemic H1N1 and other 5 internal genes of triple reassortant swine origin (TTTTPT). Pigs experimentally infected with H3.2010.2 demonstrated efficient nasal shedding and replication in the lungs, mild pneumonia, minimal microscopic lung lesions and transmitted the virus to indirect contact swine. Antigenically, H3.2010.2 viruses were closer to a human seasonal vaccine strain A/Hong Kong/4801/2014 compared to the H3.2010.1 viruses. This was the second sustained transmission of a human seasonal IAV into swine from the 2010 decade after H3.2010.1. Monitoring the spillover and detection of novel IAV from humans to swine may help vaccine antigen selection and could impact pandemic preparedness.