Aerosol transmission from infected swine to ferrets of a swine H3N2 virus collected from an agricultural fair and associated with human variant infections

Authors: KAPLAN, BRYAN - Oak Ridge Institute For Science And Education (ORISE); KIMBLE, J - Oak Ridge Institute For Science And Education (ORISE); CHANG, JENNIFER - Oak Ridge Institute For Science And Education (ORISE); Anderson, Tavis; GAUGER, PHILLIP - Iowa State University; JANAS-MARTINDALE, ALICIA - Animal And Plant Health Inspection Service (APHIS); KILLIAN, MARY LEA - Animal And Plant Health Inspection Service (APHIS); BOWMAN, ANDREW - The Ohio State University; Baker, Amy

Submitted to: Journal of Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/28/2020
Publication Date: 6/10/2020
Publication URL: https://handle.nal.usda.gov/10113/7019786
Citation: Kaplan, B.S., Kimble, J.B., Chang, J., Anderson, T.K., Gauger, P., Janas-Martindale, A., Killian, M., Bowman, A.S., Vincent, A.L. 2020. Aerosol transmission from infected swine to ferrets of a swine H3N2 virus collected from an agricultural fair and associated with human variant infections. Journal of Virology. https://doi.org//10.1128/JVI.01009-20.
DOI: https://doi.org/10.1128/JVI.01009-20

Interpretive Summary: The transmission of influenza A viruses (IAV) from swine to humans occurs sporadically and is often associated with agricultural fairs in the USA. Swine origin IAV that are detected in humans are called "variant" to differentiate from human seasonal IAV. During the 2016-2017 influenza season, 61 H3N2 variant (H3N2v) cases were reported. We compared the genomes of human H3N2v viruses and swine H3N2 viruses collected at the same state fair in Ohio. The genomes of the swine and human viruses were 100% identical. To better understand the ability of these H3N2 viruses to transmit from swine to humans, we infected pigs with an H3N2 virus from the 2017 fair outbreak, and placed them in an enclosure in close proximity to caged ferrets, the gold-standard model of human influenza virus infection and transmission. The swine H3N2 replicated in pigs and the ferrets that were exposed to the infectious, respiratory aerosols of the pigs. An additional group of ferrets were directly infected with the H3N2 virus. These results are the first to show the ability of the 2017 H3N2 virus to transmit efficiently from swine to ferrets without the need of any modification to the virus.

Technical Abstract: Influenza A viruses (IAV) sporadically transmit from swine to humans, typically associated with agricultural fairs in the USA. A human seasonal H3 from the 2010-2011 IAV season was introduced into the US swine population and termed H3.2010.1 to differentiate from the previous swine H3. This H3N2 lineage became widespread in the US commercial swine population, subsequently spilling over into exhibition swine, and caused a majority of H3N2 variant (H3N2v) cases in humans in 2016 and 2017. A cluster of human H3N2v cases were reported at an agricultural fair in Ohio in 2017 where 2010.1 H3N2 IAV was concurrently detected in exhibition swine. Genomic analysis showed the swine and human isolates were nearly identical. Here we evaluated the propensity of a 2010.1 H3N2 IAV (A/swine/Ohio/A01354299/2017; OH/2017) isolated from the agricultural fair outbreak to replicate in ferrets and transmit from swine to ferret. OH/2017 displayed robust replication in the ferret respiratory tract, causing slight fever and moderate weight loss. Further, OH/2017 was capable of efficient respiratory droplet transmission from infected pigs to contact ferrets. These findings emphasize the need for enhanced surveillance of influenza in exhibition swine as well as the continued development of more effective vaccines or other control measures to limit the dissemination of viruses in the exhibition swine population and to reduce the risk of zoonotic infections.