A 2018-2019 human seasonal H3N2 influenza A virus spillover into swine with demonstrated virus transmission in pigs

Authors: POWELL, JOSHUA - Oak Ridge Institute For Science And Education (ORISE); Anderson, Tavis; ZELLER, MICHAEL - Iowa State University; GAUGER, PHILLIP - Iowa State University; Baker, Amy

Submitted to: Journal of Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/14/2024
Publication Date: N/A
Citation: N/A

Interpretive Summary: Interspecies human-to-swine IAV transmission occurs globally and contributes to increased IAV diversity in pig populations. We present data that a swine isolate from a 2018-2019 human-to-swine transmission event was shed for multiple days in challenged and contact pigs. By characterizing this introduction through bioinformatic, molecular, and animal experimental approaches, these findings better inform animal health policy in candidate vaccine decision-making. Since wholly human seasonal H3N2 viruses in the U.S. did not easily spread to and among pigs in the past, these findings reveal the barriers for transmission from people into pigs may not require significant changes in all human seasonal H3N2.

Technical Abstract: Four detections of human seasonal H3 3C3a clade origin influenza A virus (IAV) were detected in 2019 in U.S. pigs from Michigan, Illinois, and Virginia. To evaluate the relative risk of this spillover to the pig population, whole genome sequencing and phylogenetic characterization was conducted and revealed all eight viral gene segments were closely related to 2018-2019 H3N2 human seasonal IAV. Next, a series of in vitro viral kinetics, receptor binding, and antigenic characterization studies were performed using a representative A/swine/Virginia/A02478738/2018(H3N2) (SW/VA/19) isolate. Viral replication kinetic studies of SW/VA/19 demonstrated less efficient replication curves than all ten swine H3N2 viruses tested, but higher than three human H3N2 strains. Serial passaging experiments of SW/VA/19 in swine cells did not increase virus replication, but changes at HA amino acid positions 9 and 159 occurred. In swine transmission studies, SW/VA/19 was shed in nasal secretions and transmitted to all indirect contact pigs, whereas the human seasonal strain A/Switzerland/9715293/2013(H3N2) from the same 3C3a clade failed to transmit. SW/VA/19 induced minimal macroscopic and microscopic lung lesions. Collectively these findings demonstrate that these human seasonal H3N2 3C3a-like viruses did not require reassortment with endemic swine IAV gene segments to facilitate virus shedding and transmission in pigs. However, limited detections in the U.S. pig population in the subsequent period of time suggests a yet unknown restriction factor likely limiting the spread of these viruses in the U.S. pig population.