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      Genomic diversity and evolutionary dynamics of Influenza A viruses in Colombian swine: implications for one health surveillance and control

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          ABSTRACT

          Influenza A viruses (IAV) impose significant respiratory disease burdens in both swine and humans worldwide, with frequent human-to-swine transmission driving viral evolution in pigs and highlighting the risk at the animal-human interface. Therefore, a comprehensive One Health approach (interconnection among human, animal, and environmental health) is needed for IAV prevention, control, and response. Animal influenza genomic surveillance remains limited in many Latin American countries, including Colombia. To address this gap, we genetically characterized 170 swine specimens from Colombia (2011–2017). Whole genome sequencing revealed a predominance of pandemic-like H1N1 lineage, with a minority belonging to H3N2 and H1N2 human seasonal-like lineage and H1N1 early classical swine lineages. Significantly, we have identified reassortant and recombinant viruses (H3N2, H1N1) not previously reported in Colombia. This suggests a broad genotypic viral diversity, likely resulting from reassortment between classical endemic viruses and new introductions established in Colombia's swine population (e.g. the 2009 H1N1 pandemic). Our study highlights the importance of a One Health approach in disease control, particularly in an ecosystem where humans are a main source of IAV to swine populations, and emphasizes the need for continued surveillance and enhanced biosecurity measures. The co-circulation of multiple subtypes in regions with high swine density facilitates viral exchange, underscoring the importance of monitoring viral evolution to inform vaccine selection and public health policies locally and globally.

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          Most cited references63

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          GISAID’s Role in Pandemic Response

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            Origins of the 2009 H1N1 influenza pandemic in swine in Mexico

            Asia is considered an important source of influenza A virus (IAV) pandemics, owing to large, diverse viral reservoirs in poultry and swine. However, the zoonotic origins of the 2009 A/H1N1 influenza pandemic virus (pdmH1N1) remain unclear, due to conflicting evidence from swine and humans. There is strong evidence that the first human outbreak of pdmH1N1 occurred in Mexico in early 2009. However, no related swine viruses have been detected in Mexico or any part of the Americas, and to date the most closely related ancestor viruses were identified in Asian swine. Here, we use 58 new whole-genome sequences from IAVs collected in Mexican swine to establish that the swine virus responsible for the 2009 pandemic evolved in central Mexico. This finding highlights how the 2009 pandemic arose from a region not considered a pandemic risk, owing to an expansion of IAV diversity in swine resulting from long-distance live swine trade. DOI: http://dx.doi.org/10.7554/eLife.16777.001
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              The M segment of the 2009 new pandemic H1N1 influenza virus is critical for its high transmission efficiency in the guinea pig model.

              A remarkable feature of the 2009 pandemic H1N1 influenza virus is its efficient transmissibility in humans compared to that of precursor strains from the triple-reassortant swine influenza virus lineage, which cause only sporadic infections in humans. The viral components essential for this phenotype have not been fully elucidated. In this study, we aimed to determine the viral factors critical for aerosol transmission of the 2009 pandemic virus. Single or multiple segment reassortments were made between the pandemic A/California/04/09 (H1N1) (Cal/09) virus and another H1N1 strain, A/Puerto Rico/8/34 (H1N1) (PR8). These viruses were then tested in the guinea pig model to understand which segment of Cal/09 virus conferred transmissibility to the poorly transmissible PR8 virus. We confirmed our findings by generating recombinant A/swine/Texas/1998 (H3N2) (sw/Tx/98) virus, a representative triple-reassortant swine virus, containing segments of the Cal/09 virus. The data showed that the M segment of the Cal/09 virus promoted aerosol transmissibility to recombinant viruses with PR8 and sw/Tx/98 virus backgrounds, suggesting that the M segment is a critical factor supporting the transmission of the 2009 pandemic virus.
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                Author and article information

                Journal
                Emerg Microbes Infect
                Emerg Microbes Infect
                Emerging Microbes & Infections
                Taylor & Francis
                2222-1751
                19 June 2024
                2024
                19 June 2024
                : 13
                : 1
                : 2368202
                Affiliations
                [a ]GHI One Health Colombia, Universidad Nacional de Colombia , Medellín, Colombia
                [b ]Pig Improvement Company , Hendersonville, NC, USA
                [c ]PorkColombia Association , Bogotá, Colombia
                [d ]Faculty of Life Sciences, Universidad Nacional de Colombia , Medellín, Colombia
                [e ]Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin , Madison, WI, USA
                [f ]Global Health Institute, University of Wisconsin , Madison, WI, USA
                Author notes
                [CONTACT ] Karl Ciuoderis coord_cwohc@ 123456unal.edu.co GHI One Health Colombia, Universidad Nacional de Colombia , Medellín, Colombia
                [*]

                These authors contributed equally to this work

                Supplemental data for this article can be accessed online at https://doi.org/10.1080/22221751.2024.2368202

                Author information
                https://orcid.org/0009-0005-2830-908X
                https://orcid.org/0000-0003-2258-4724
                https://orcid.org/0000-0003-0404-9947
                Article
                2368202
                10.1080/22221751.2024.2368202
                11229761
                38970562
                afb7e6c1-90d0-47ed-83fb-2404bdf04c9e
                © 2024 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, on behalf of Shanghai Shangyixun Cultural Communication Co., Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the Accepted Manuscript in a repository by the author(s) or with their consent.

                History
                Page count
                Figures: 5, Tables: 2, Equations: 0, References: 69, Pages: 14
                Categories
                Emerging Seasonal and Pandemic Influenza Infections
                Research Article

                influenza a viruses,swine health,genetic characterization,colombia,reassortment,one health

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