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Abstract
To assess the current status of influenza A viruses of swine (IAVs-S) throughout Japan and to investigate how these viruses persisted and evolve on pig farms, we genetically characterized IAVs-S isolated during 2015 to 2019. Nasal swab samples collected through active surveillance and lung tissue samples collected for diagnosis yielded 424 IAVs-S, comprising 78 H1N1, 331 H1N2, and 15 H3N2 viruses, from farms in 21 sampled prefectures in Japan. Phylogenetic analyses of surface genes revealed that the 1A.1 classical swine H1 lineage has evolved uniquely since the late 1970s among pig populations in Japan. During 2015 to 2019, A(H1N1)pdm09 viruses repeatedly became introduced into farms and reassorted with endemic H1N2 and H3N2 IAVs-S. H3N2 IAVs-S isolated during 2015 to 2019 formed a clade that originated from 1999-2000 human seasonal influenza viruses; this situation differs from previous reports, in which H3N2 IAVs-S derived from human seasonal influenza viruses were transmitted sporadically from humans to swine but then disappeared without becoming established within the pig population. At farms where IAVs-S were frequently isolated for at least 3 years, multiple introductions of IAVs-S with phylogenetically distinct hemagglutinin (HA) genes occurred. In addition, at one farm, IAVs-S derived from a single introduction persisted for at least 3 years and carried no mutations at the deduced antigenic sites of the hemagglutinin protein, except for one at the antigenic site (Sa). Our results extend our understanding regarding the status of IAVs-S currently circulating in Japan and how they genetically evolve at the farm level.IMPORTANCE Understanding the current status of influenza A viruses of swine (IAVs-S) and their evolution at the farm level is important for controlling these pathogens. Efforts to monitor IAVs-S during 2015 to 2019 yielded H1N1, H1N2, and H3N2 viruses. H1 genes in Japanese swine formed a unique clade in the classical swine H1 lineage of 1A.1, and H3 genes originating from 1999-2000 human seasonal influenza viruses appear to have become established among Japanese swine. A(H1N1)pdm09-derived H1 genes became introduced repeatedly and reassorted with endemic IAVs-S, resulting in various combinations of surface and internal genes among pig populations in Japan. At the farm level, multiple introductions of IAVs-S with phylogenetically distinct HA sequences occurred, or IAVs-S derived from a single introduction have persisted for at least 3 years with only a single mutation at the antigenic site of the HA protein. Continued monitoring of IAVs-S is necessary to update and maximize control strategies.
Highlights
To assess the current status of influenza A viruses of swine (IAVs-S) throughout Japan and to investigate how these viruses persisted and evolve on pig farms, we genetically characterized IAVs-S isolated during 2015 to 2019
In 1998, a triplereassortant H3N2 virus emerged in North America through reassortment among a human seasonal virus, a classical swine Influenza A virus of swine (IAV-S), and an avian influenza virus, which was followed by the emergence of H1N1 and H1N2 triple-reassortant IAVs-S and their circulation in North America
human seasonal H3 and N2 genes (H-H) H3N2 IAVs-S were isolated from 3 prefectures on Kyushu (Kagoshima, Miyazaki, and Nagasaki) and from Chiba prefecture. Gene constellations and their numbers in the present study revealed all IAVs-S isolated here had at least 1 gene that was derived from an A(H1N1)pdm09 virus, except for a single strain isolated in Tochigi prefecture: A/swine/Tochigi/38-7119/2019 (H1N2) inherited all of its genes from Japanese pig isolates that circulated during the 1990s and 2000s (Fig. 5 and Fig. S9)
Summary
To assess the current status of influenza A viruses of swine (IAVs-S) throughout Japan and to investigate how these viruses persisted and evolve on pig farms, we genetically characterized IAVs-S isolated during 2015 to 2019. Classical swine H1N1 IAVs-S were first isolated in North America in 1930 and have been infecting pigs endemically there since the 1970s, currently circulating among pig population worldwide, whereas avian-like H1N1 IAVs-S have stably persisted in Europe since 1979 [7, 8]. In April 2009, an IAV containing a combination of segments from both the above-described triple-reassortant virus and Eurasian avian-like swine lineages spread rapidly to cause a worldwide pandemic in humans [23, 24]. After the 2009 pandemic, A(H1N1)pdm viruses were introduced into swine populations and reassorted with endemic IAVs-S, further increasing genetic diversity among IAVs-S all over the world [25,26,27,28,29,30,31,32,33,34,35,36,37]
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