Introductions of human-origin seasonal H3N2, H1N2, and pre-2009 H1N1 influenza viruses to swine in Brazil

Authors: TOCHETTO, CAROL - Embrapa; JUNQUEIRA, DENNIS - Universidade Federal De Santa Maria; Anderson, Tavis; GAVA, DANIELLE - Embrapa; HAACH, VANESSA - Federal University Of Rio Grande Do Sul; CANTAO, MAURICIO - Embrapa; Baker, Amy; SCHAEFER, REJANE - Embrapa

Submitted to: Viruses
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/16/2023
Publication Date: 2/19/2023
Citation: Tochetto, C., Junqueira, D.M., Anderson, T.K., Gava, D., Haach, V., Cantao, M.E., Baker, A.L., Schaefer, R. 2023. Introductions of human-origin seasonal H3N2, H1N2, and pre-2009 H1N1 influenza viruses to swine in Brazil. Viruses. 15(2). Article 576. https://doi.org/10.3390/v15020576.
DOI: https://doi.org/10.3390/v15020576

Interpretive Summary: Pigs can be infected with influenza A viruses (IAV) from multiple species, and frequent human-to-swine transmission has contributed to the diversity of IAV in swine populations around the globe. We conducted surveillance for IAV in pigs in Brazil during 2011-2020 and isolated and characterized 107 H1N1, H1N2 and H3N2 IAVs. These data revealed eight introductions of HA and NA gene segments derived from human seasonal IAV into swine in Brazil since the 1980s. A subset of these introductions have persisted and evolved, including three H1 subtype genetic lineages, and one H3 subtype genetic lineage that has diversified into three different groups. All these introductions resulted in IAV that appear to circulate only in Brazilian swine herds. The identification of these viruses demonstrates the importance of a robust surveillance system for IAV in swine to inform control measures. These data can be used for objective vaccine and diagnostic updates, as well as help identify factors to prevent infection and transmission, such as changes in production practices or on-farm management.

Technical Abstract: Several lineages of antigenically and genetically distinct influenza A virus (IAV) circulate in swine populations globally. In South America, the evolutionary history of influenza A virus (IAV) in swine has been obscured by historically low levels of surveillance, and this has hampered control measures and assessment of the zoonotic risk of emerging viruses. Although only H1N1, H1N2, and H3N2 IAV subtypes are enzootic in pigs, hemagglutinin (HA) and neuraminidase (NA) genes have shown an enormous diversity which is mainly the result of bidirectional transmission of IAVs between human and swine. We conducted surveillance for IAV in pigs in Brazil during 2011-2020 and isolated and characterized 107 H1N1, H1N2 and H3N2 IAVs. Phylogenetic analysis with a representative data set of human and swine IAV revealed evidence of eight introductions of HA and NA gene segments derived from human seasonal IAV that have occurred since the mid-late 1980s and remained undetected in swine for decades. Additionally, our analyses revealed three genetic clades of H1 within 1B lineage originated from three distinct spillover events (clades 1B.2.3, 1B.2.4 and 1B.2.6), and an H3 lineage that has diversified into three genetic clades (H3 1990.5.1, 1990.5.2 and 1990.5.3). The N2 segment from human seasonal H1N2 and H3N2 viruses was introduced into swine six times and a single introduction of an N1 segment from human H1N1 virus was identified. The analysis of the internal gene segments revealed evidence for additional reassortment with H1N1pdm09 viruses. Notably, all these introductions resulted in IAV that apparently circulate only in Brazilian swine herds. Future analysis may reveal when and how reassortment between endemic swine IAV and the novel human spillover viruses has resulted in the persistence of seven lineages in Brazilian swine. These results reinforce the significant contributions of human IAVs to the genetic diversity of IAV in swine and reiterate the importance of surveillance of IAV in pigs.