Introductions of Human-Origin Seasonal H3N2, H1N2 and Pre-2009 H1N1 Influenza Viruses to Swine in Brazil

Abstract

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 the assessment of the zoonotic risk of emerging viruses. The extensive genetic diversity of IAV in swine observed globally has been attributed mainly to bidirectional transmission between humans and pigs. We conducted surveillance in swine in Brazil during 2011–2020 and characterized 107 H1N1, H1N2, and H3N2 IAVs. Phylogenetic analysis based on HA and NA segments revealed that human seasonal IAVs were introduced at least eight times into swine in Brazil since the mid-late 1980s. Our analyses revealed three genetic clades of H1 within the 1B lineage originated from three distinct spillover events, and an H3 lineage that has diversified into three genetic clades. 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 the human H1N1 virus was identified. Additional analysis revealed further reassortment with H1N1pdm09 viruses. All these introductions resulted in IAVs that apparently circulate only in Brazilian herds. 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.

Human-to-swine introductions and onward transmission of 2009 H1N1 pandemic influenza viruses in Brazil

“…Subsequently, surveillance efforts for detection of IAV in swine populations have increased in the last decade, especially through the efforts made by the Brazilian Agricultural Research Corporation (EMBRAPA Swine and Poultry). As a result, at least eight introductions of human seasonal H1N1, H1N2, and H3N2 viruses were detected in swine in Brazil, along with H1N1pdm09 ( Tochetto et al, 2023 ). Most of these introductions had sustained onward transmission in swine prior to 2009, followed by reassortment with H1N1pdm09 lineage viruses.…”

Antigenic and genetic diversity of H1 and H3 influenza A viruses in swine in Brazil

“…and introductions in the early 2000s for the 1B lineage (1B.2.3 and 1B.2.4) and subsequent circulation of these viruses within Brazilian pig populations (8)(9)(10). Antigenic analysis of the Brazilian 1A lineage revealed a complex spatial distribution of antigenic diversity across the lineage.…”

“…Surveillance and characterization of the genetic and antigenic diversity of swine IAVs in Brazil has been increasing since the H1N1 pandemic of 2009 (6,(8)(9)(10)37).…”

“…Brazil is the fourth largest pork producer and exporter in the world; however, there are few reports describing circulation of IAVs in Brazilian swine populations prior to the 2009 pandemic (6, 7). Previous work identified multiple human-to-swine spill-overs of seasonal H3 and H1 influenza A virus strains into pigs in Brazil (8, 9). Genes from these spillovers persisted in Brazilian swine and the internal gene cassette of these viruses has changed through reassortment with the A(H1N1)pdm09 that now also co-circulates within the swine population (9, 10).…”

“…Previous work identified multiple human-to-swine spill-overs of seasonal H3 and H1 influenza A virus strains into pigs in Brazil (8, 9). Genes from these spillovers persisted in Brazilian swine and the internal gene cassette of these viruses has changed through reassortment with the A(H1N1)pdm09 that now also co-circulates within the swine population (9, 10). The impact of reassortment and cocirculating lineages of viruses on antigenic diversity in Brazilian pigs is unresolved.…”