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. 2024 Dec 30;15(1):10748.
doi: 10.1038/s41467-024-53815-z.

Zoonotic transmission of novel Influenza A variant viruses detected in Brazil during 2020 to 2023

Paola Cristina Resende #  1 , Dennis M Junqueira #  2 , Caroline Tochetto #  3 , Maria Ogrzewalska  4 , Fernando C Motta  4 , Jonathan Lopes  4 , Luciana Appolinario  4 , Larissa Macedo  4 , Braulia Caetano  4 , Aline Matos  4 , Thauane Silva  4 , Elisa Cavalcante Pereira  4 , Leticia Ferreira Lima  4 , Irina Riediger  5 , Maria do Carmo Debur  5 , Guilherme Nardi Becker  5 , Aline Andrade  5 , Acácia Maria Lourenço Francisco Nasr  6 , Rosana Aparecida Piler  6 , Ana Carolina Dalla Vecchia  6 , Walquíria Almeida  7 , David Brown  4 , Rejane Schaefer  3 , Marilda M Siqueira  4
Affiliations

Zoonotic transmission of novel Influenza A variant viruses detected in Brazil during 2020 to 2023

Paola Cristina Resende et al. Nat Commun. .

Abstract

Zoonotic infections (swine-human) caused by influenza A viruses (IAVs) have been reported and linked to close contact between these species. Here, we describe eight human IAV variant infections (6 mild and 2 severe cases, including 1 death) detected in Paraná, Brazil, during 2020-2023. Genomes recovered were closely related to Brazilian swIAVs of three major lineages (1 A.3.3.2/pdm09, 1B/human-like, and H3.1990.5), including three H1N1v, two H1N2v, two H3N2v and one H1v. Five H1v were closely related to pdm09 lineage, one H1v (H1N2v) grouped within 1B.2.3 clade, and the two H3v grouped within a clade composed exclusively of Brazilian H3 swIAV (clade H3.1990.5.1). Internal gene segments were closely related to H1N1pdm09 isolated from pigs. IAV variant rarely result in sustained transmission between people, however the potential to develop such ability is of concern and must not be underestimated. This study brings into focus the need for continuous influenza surveillance and timely risk assessment.

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Conflict of interest statement

Competing interests: The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Geographic and sample information of eight influenza A variant viruses collected from human infections in Brazil.
a Locations in the State of Paraná, Brazil, where cases were detected. Concentric circles depict the proportion of cases identified in each location. b Genetic composition of viruses identified in the swine-to-human transmissions. The vertical bars correspond to the colors of the locations in (a). Horizontal bars identify the eight genomic segments of IAVs: (i) PB2, (ii) PB1, (iii) PA, (iv) HA, (v) NP, (vi) NA, (vii) MP, and (viii) NS. The figure key shows the subtype of each segment.
Fig. 2
Fig. 2. Maximum Likelihood phylogenetic tree inferred for 374 H1 hemagglutinin gene sequences of pre-2009 human influenza A viruses, and swine influenza A viruses collected globally from 1977 to 2020, including the H1v described in this study, A/Parana/3625/2020(H1N2)v (Case 1).
Swine sequences isolated in Brazil contains the state of isolation within its names (Brazil_MG = Minas Gerais, Brazil_MS = Mato Grosso do Sul, Brazil_PR = Paraná, Brazil_RS = Rio Grande do Sul, Brazil_SC = Santa Catarina, Brazil_SP = São Paulo). Branches are colored by host as shown in the figure key. The tree is midpoint rooted for clarity, and all branch lengths are drawn to scale representing nucleotide substitutions per site. Black-circles at the internal nodes identify clades supported by SH-aLRT > 80% and/or UFB > 95%. A Phylogenetic tree showing the three genetic clades of H1 viruses of the 1B lineage that circulate in swine in Brazil (1B.2.3, 1B.2.4, and 1B.2.6). The swine-to-human introduction is highlighted by a gray-shaded form. B Topology details for Clade H1 1B.2.3 that comprises the HA of A/Parana/3625/2020(H1N2)v.
Fig. 3
Fig. 3. Maximum Likelihood phylogenetic tree inferred for 3209 N2 neuraminidase gene sequences of influenza A viruses collected worldwide from 1969 to 2022, and including the three N2v described in this study, A/Parana/3625/2020(H1N2)v (Case 1), A/Parana/28600/2020(H1N2)v (Case 2), and A/Parana/51528/2021(H3N2)v (Case 5).
Swine sequences isolated in Brazil contains the state of isolation within its names (Brazil_PR = Paraná, Brazil_RS = Rio Grande do Sul, Brazil_SC = Santa Catarina). The tree is midpoint rooted for clarity. Branches are colored by host and cases are color-coded according to the figure key. Branch lengths are drawn to scale representing nucleotide substitutions per site. Black-circles at the internal nodes identify clades supported by SH-aLRT > 80% and/or UFB > 95%. A Phylogenetic tree indicating the swine-to-human introductions occurred in Brazil by gray-shaded forms. B Topology details for N2 #4 Brazilian clade. C Topology details for N2 #2 Brazilian clade.
Fig. 4
Fig. 4. Maximum Likelihood phylogenetic tree inferred for 2853 H1pdm09 hemagglutinin gene sequences collected worldwide from 2009 to 2023 and including five H1pdm09v isolated in this study (A/Parana/10835/2021, A/Parana/20675/2022, A/Parana/5210/2023, A/Parana/28600/2020, and A/Parana/13897/2023).
Swine sequences isolated in Brazil contains the state of isolation within its names (Brazil_PR = Paraná, Brazil_RS = Rio Grande do Sul, Brazil_SC = Santa Catarina,). Branches are colored by host and cases are color-coded according to the figure key. Branch lengths are drawn to scale representing nucleotide substitutions per site. Black-circles at the internal nodes identify clades supported by SH-aLRT > 80%. A Phylogenetic tree indicating swine-to-human introductions occurred in Brazil by gray-shaded forms. B Topology details for Clades H1 pdm #1 and #2. c Topology details for Clade H1 pdm #3.
Fig. 5
Fig. 5. Maximum likelihood phylogenetic tree inferred for 2159 N1pdm09 neuraminidase gene sequences collected worldwide from 2009 to 2023 and including three N1pdm09v isolated in this study (A/Parana/10835/2021, A/Parana/20675/2022, and A/Parana/13897/2023).
Swine sequences isolated in Brazil contains the state of isolation within its names (Brazil_MG = Minas Gerais, Brazil_PR = Paraná, Brazil_RS = Rio Grande do Sul, Brazil_SC = Santa Catarina). Branches are colored by host and cases are color-coded according to the figure key. Branch lengths are drawn to scale representing nucleotide substitutions per site. Black-circles at the internal nodes identify clades supported by SH-aLRT > 80%. A Phylogenetic tree indicating swine-to-human introductions occurred in Brazil by gray-shaded forms. B Topology details for Clade N1 pdm #1.
Fig. 6
Fig. 6. Maximum Likelihood phylogenetic tree inferred for 3661 H3 hemagglutinin gene sequences of influenza A viruses collected worldwide from 1973 to 2023, and including the two H3v obtained in this study, A/Parana/44707/2021(H3N2)v (Case 4) and A/Parana/51528/2021(H3N2)v (Case 5).
Swine sequences isolated in Brazil contains the state of isolation within its names (Brazil_MG = Minas Gerais, Brazil_MS = Mato Grosso do Sul, Brazil_PR = Paraná, Brazil_RS = Rio Grande do Sul, Brazil_SC = Santa Catarina, Brazil_SP = São Paulo). Branches are colored by host and cases are color-coded according to the figure key. The tree is midpoint rooted for clarity, and all branch lengths are drawn to scale representing nucleotide substitutions per site. Black-circles at the internal nodes identify clades supported by SH-aLRT > 80% and/or UFB > 95%. A Phylogenetic tree showing the major clade of H3 viruses that circulate in swine in Brazil (H3 1990.5). The swine-to-human introduction is highlighted by a gray-shaded form. B Topology details of the H3 Brazilian clade and subclades (1990.5.1, 1990.5.2, and 1990.5.3), with emphasis on the variant viruses.
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