High pathogenic avian influenza A(H5) viruses of clade 2.3.4.4b in Europe - Why trends of virus evolution are more difficult to predict

Alice Fusaro; Bianca Zecchin; Edoardo Giussani; Elisa Palumbo; Montserrat Agüero-García; Claudia Bachofen; Ádám Bálint; Fereshteh Banihashem; Ashley C. Banyard; Nancy Beerens; Manon Bourg; Francois Xavier Briand; Caroline Bröjer; Ian H. Brown; Brigitte Brugger; Alexander M.P. Byrne; Armend Cana; Vasiliki Christodoulou; Zuzana Dirbakova; Teresa Fagulha; Ron A.M. Fouchier; Laura Garza-Cuartero; George Georgiades; Britt Gjerset; Beatrice Grasland; Oxana Groza; Timm Harder; Ana Margarida Henriques; Charlotte Kristiane Hjulsager; Emiliya Ivanova; Zygimantas Janeliunas; Laura Krivko; Ken Lemon; Yuan Liang; Aldin Lika; Peter Malik; Michael J. Mcmenamy; Alexander Nagy; Imbi Nurmoja; Iuliana Onita; Anne Pohlmann; Sandra Revilla-Fernández; Azucena Sánchez-Sánchez; Vladimir Savic; Brigita Slavec; Krzysztof Smietanka; Chantal J. Snoeck; Mieke Steensels; Vilhjálmur Svansson; Edyta Swieton; Niina Tammiranta; Martin Tinak; Steven Van Borm; Siamak Zohari; Cornelia Adlhoch; Francesca Baldinelli; Calogero Terregino; Isabella Monne

doi:10.1093/ve/veae027

High pathogenic avian influenza A(H5) viruses of clade 2.3.4.4b in Europe - Why trends of virus evolution are more difficult to predict

Alice Fusaro^*, Bianca Zecchin, Edoardo Giussani, Elisa Palumbo, Montserrat Agüero-García, Claudia Bachofen, Ádám Bálint, Fereshteh Banihashem, Ashley C. Banyard, Nancy Beerens, Manon Bourg, Francois Xavier Briand, Caroline Bröjer, Ian H. Brown, Brigitte Brugger, Alexander M.P. Byrne, Armend Cana, Vasiliki Christodoulou, Zuzana Dirbakova, Teresa FagulhaRon A.M. Fouchier, Laura Garza-Cuartero, George Georgiades, Britt Gjerset, Beatrice Grasland, Oxana Groza, Timm Harder, Ana Margarida Henriques, Charlotte Kristiane Hjulsager, Emiliya Ivanova, Zygimantas Janeliunas, Laura Krivko, Ken Lemon, Yuan Liang, Aldin Lika, Peter Malik, Michael J. Mcmenamy, Alexander Nagy, Imbi Nurmoja, Iuliana Onita, Anne Pohlmann, Sandra Revilla-Fernández, Azucena Sánchez-Sánchez, Vladimir Savic, Brigita Slavec, Krzysztof Smietanka, Chantal J. Snoeck, Mieke Steensels, Vilhjálmur Svansson, Edyta Swieton, Niina Tammiranta, Martin Tinak, Steven Van Borm, Siamak Zohari, Cornelia Adlhoch, Francesca Baldinelli, Calogero Terregino, Isabella Monne

^*Corresponding author for this work

Clinical and Applied Virology

Research output: Contribution to journal › Article › Research › peer-review

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Abstract

Since 2016, A(H5Nx) high pathogenic avian influenza (HPAI) virus of clade 2.3.4.4b has become one of the most serious global threats not only to wild and domestic birds, but also to public health. In recent years, important changes in the ecology, epidemiology, and evolution of this virus have been reported, with an unprecedented global diffusion and variety of affected birds and mammalian species. After the two consecutive and devastating epidemic waves in Europe in 2020-2021 and 2021-2022, with the second one recognized as one of the largest epidemics recorded so far, this clade has begun to circulate endemically in European wild bird populations. This study used the complete genomes of 1,956 European HPAI A(H5Nx) viruses to investigate the virus evolution during this varying epidemiological outline. We investigated the spatiotemporal patterns of A(H5Nx) virus diffusion to/from and within Europe during the 2020-2021 and 2021-2022 epidemic waves, providing evidence of ongoing changes in transmission dynamics and disease epidemiology. We demonstrated the high genetic diversity of the circulating viruses, which have undergone frequent reassortment events, providing for the first time a complete overview and a proposed nomenclature of the multiple genotypes circulating in Europe in 2020-2022. We described the emergence of a new genotype with gull adapted genes, which offered the virus the opportunity to occupy new ecological niches, driving the disease endemicity in the European wild bird population. The high propensity of the virus for reassortment, its jumps to a progressively wider number of host species, including mammals, and the rapid acquisition of adaptive mutations make the trend of virus evolution and spread difficult to predict in this unfailing evolving scenario.

Original language	English
Article number	veae027
Journal	Virus Evolution
Volume	10
Issue number	1
DOIs	https://doi.org/10.1093/ve/veae027
Publication status	Published - 6 Apr 2024

Keywords

Europe
high pathogenic avian influenza A(H5) viruses
phylodynamics
reassortments
spatial spread

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10.1093/ve/veae027Licence: CC BY-NC

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Fusaro, A., Zecchin, B., Giussani, E., Palumbo, E., Agüero-García, M., Bachofen, C., Bálint, Á., Banihashem, F., Banyard, A. C., Beerens, N., Bourg, M., Briand, F. X., Bröjer, C., Brown, I. H., Brugger, B., Byrne, A. M. P., Cana, A., Christodoulou, V., Dirbakova, Z., ... Monne, I. (2024). High pathogenic avian influenza A(H5) viruses of clade 2.3.4.4b in Europe - Why trends of virus evolution are more difficult to predict. Virus Evolution, 10(1), Article veae027. https://doi.org/10.1093/ve/veae027

@article{46fa0f9ae9814b2ea4081dce0673661e,

title = "High pathogenic avian influenza A(H5) viruses of clade 2.3.4.4b in Europe - Why trends of virus evolution are more difficult to predict",

abstract = "Since 2016, A(H5Nx) high pathogenic avian influenza (HPAI) virus of clade 2.3.4.4b has become one of the most serious global threats not only to wild and domestic birds, but also to public health. In recent years, important changes in the ecology, epidemiology, and evolution of this virus have been reported, with an unprecedented global diffusion and variety of affected birds and mammalian species. After the two consecutive and devastating epidemic waves in Europe in 2020-2021 and 2021-2022, with the second one recognized as one of the largest epidemics recorded so far, this clade has begun to circulate endemically in European wild bird populations. This study used the complete genomes of 1,956 European HPAI A(H5Nx) viruses to investigate the virus evolution during this varying epidemiological outline. We investigated the spatiotemporal patterns of A(H5Nx) virus diffusion to/from and within Europe during the 2020-2021 and 2021-2022 epidemic waves, providing evidence of ongoing changes in transmission dynamics and disease epidemiology. We demonstrated the high genetic diversity of the circulating viruses, which have undergone frequent reassortment events, providing for the first time a complete overview and a proposed nomenclature of the multiple genotypes circulating in Europe in 2020-2022. We described the emergence of a new genotype with gull adapted genes, which offered the virus the opportunity to occupy new ecological niches, driving the disease endemicity in the European wild bird population. The high propensity of the virus for reassortment, its jumps to a progressively wider number of host species, including mammals, and the rapid acquisition of adaptive mutations make the trend of virus evolution and spread difficult to predict in this unfailing evolving scenario.",

keywords = "Europe, high pathogenic avian influenza A(H5) viruses, phylodynamics, reassortments, spatial spread",

author = "Alice Fusaro and Bianca Zecchin and Edoardo Giussani and Elisa Palumbo and Montserrat Ag{\"u}ero-Garc{\'i}a and Claudia Bachofen and {\'A}d{\'a}m B{\'a}lint and Fereshteh Banihashem and Banyard, {Ashley C.} and Nancy Beerens and Manon Bourg and Briand, {Francois Xavier} and Caroline Br{\"o}jer and Brown, {Ian H.} and Brigitte Brugger and Byrne, {Alexander M.P.} and Armend Cana and Vasiliki Christodoulou and Zuzana Dirbakova and Teresa Fagulha and Fouchier, {Ron A.M.} and Laura Garza-Cuartero and George Georgiades and Britt Gjerset and Beatrice Grasland and Oxana Groza and Timm Harder and Henriques, {Ana Margarida} and Hjulsager, {Charlotte Kristiane} and Emiliya Ivanova and Zygimantas Janeliunas and Laura Krivko and Ken Lemon and Yuan Liang and Aldin Lika and Peter Malik and Mcmenamy, {Michael J.} and Alexander Nagy and Imbi Nurmoja and Iuliana Onita and Anne Pohlmann and Sandra Revilla-Fern{\'a}ndez and Azucena S{\'a}nchez-S{\'a}nchez and Vladimir Savic and Brigita Slavec and Krzysztof Smietanka and Snoeck, {Chantal J.} and Mieke Steensels and Vilhj{\'a}lmur Svansson and Edyta Swieton and Niina Tammiranta and Martin Tinak and {Van Borm}, Steven and Siamak Zohari and Cornelia Adlhoch and Francesca Baldinelli and Calogero Terregino and Isabella Monne",

note = "Acknowledgements Support for this work was provided by the European Commission within the framework of the activities foreseen by the European Union Reference Laboratory for Avian Influenza and Newcastle Disease under grant agreement SI2.870510. This work was also partially supported by KAPPA-FLU HORIZON-CL6-2022-FARM2FORK-02-03 (grant agreement No 101084171) and FLU-SWITCH Era-Net ICRAD (grant agreement No 862605). ACB, AMPB and IHB were supported by the Biotechnology and Biological Sciences Research Council (BBSRC) and Department for Environment, Food and Rural Affairs (Defra, UK) research initiative {\textquoteleft}FluMAP{\textquoteright} [grant number BB/X006204/1]. Funding was also provided by Defra and the devolved administrations of Scotland and Wales through SE2213, SV3032 and SV3400. The authors wish to thank Francesca Ellero, Joe James and Caroline Br{\"o}jer for their careful revision of the manuscript. We gratefully acknowledge also the authors, originating and submitting laboratories of the sequences from GISAID{\textquoteright}s EpiFlu{\texttrademark} Database on which this research is based in part (Supplementary Table S4). ",

year = "2024",

month = apr,

day = "6",

doi = "10.1093/ve/veae027",

language = "English",

volume = "10",

journal = "Virus Evolution",

issn = "2057-1577",

publisher = "Oxford University Press",

number = "1",

}

Fusaro, A, Zecchin, B, Giussani, E, Palumbo, E, Agüero-García, M, Bachofen, C, Bálint, Á, Banihashem, F, Banyard, AC, Beerens, N, Bourg, M, Briand, FX, Bröjer, C, Brown, IH, Brugger, B, Byrne, AMP, Cana, A, Christodoulou, V, Dirbakova, Z, Fagulha, T, Fouchier, RAM, Garza-Cuartero, L, Georgiades, G, Gjerset, B, Grasland, B, Groza, O, Harder, T, Henriques, AM, Hjulsager, CK, Ivanova, E, Janeliunas, Z, Krivko, L, Lemon, K, Liang, Y, Lika, A, Malik, P, Mcmenamy, MJ, Nagy, A, Nurmoja, I, Onita, I, Pohlmann, A, Revilla-Fernández, S, Sánchez-Sánchez, A, Savic, V, Slavec, B, Smietanka, K, Snoeck, CJ, Steensels, M, Svansson, V, Swieton, E, Tammiranta, N, Tinak, M, Van Borm, S, Zohari, S, Adlhoch, C, Baldinelli, F, Terregino, C & Monne, I 2024, 'High pathogenic avian influenza A(H5) viruses of clade 2.3.4.4b in Europe - Why trends of virus evolution are more difficult to predict', Virus Evolution, vol. 10, no. 1, veae027. https://doi.org/10.1093/ve/veae027

TY - JOUR

T1 - High pathogenic avian influenza A(H5) viruses of clade 2.3.4.4b in Europe - Why trends of virus evolution are more difficult to predict

AU - Fusaro, Alice

AU - Zecchin, Bianca

AU - Giussani, Edoardo

AU - Palumbo, Elisa

AU - Agüero-García, Montserrat

AU - Bachofen, Claudia

AU - Bálint, Ádám

AU - Banihashem, Fereshteh

AU - Banyard, Ashley C.

AU - Beerens, Nancy

AU - Bourg, Manon

AU - Briand, Francois Xavier

AU - Bröjer, Caroline

AU - Brown, Ian H.

AU - Brugger, Brigitte

AU - Byrne, Alexander M.P.

AU - Cana, Armend

AU - Christodoulou, Vasiliki

AU - Dirbakova, Zuzana

AU - Fagulha, Teresa

AU - Fouchier, Ron A.M.

AU - Garza-Cuartero, Laura

AU - Georgiades, George

AU - Gjerset, Britt

AU - Grasland, Beatrice

AU - Groza, Oxana

AU - Harder, Timm

AU - Henriques, Ana Margarida

AU - Hjulsager, Charlotte Kristiane

AU - Ivanova, Emiliya

AU - Janeliunas, Zygimantas

AU - Krivko, Laura

AU - Lemon, Ken

AU - Liang, Yuan

AU - Lika, Aldin

AU - Malik, Peter

AU - Mcmenamy, Michael J.

AU - Nagy, Alexander

AU - Nurmoja, Imbi

AU - Onita, Iuliana

AU - Pohlmann, Anne

AU - Revilla-Fernández, Sandra

AU - Sánchez-Sánchez, Azucena

AU - Savic, Vladimir

AU - Slavec, Brigita

AU - Smietanka, Krzysztof

AU - Snoeck, Chantal J.

AU - Steensels, Mieke

AU - Svansson, Vilhjálmur

AU - Swieton, Edyta

AU - Tammiranta, Niina

AU - Tinak, Martin

AU - Van Borm, Steven

AU - Zohari, Siamak

AU - Adlhoch, Cornelia

AU - Baldinelli, Francesca

AU - Terregino, Calogero

AU - Monne, Isabella

N1 - Acknowledgements Support for this work was provided by the European Commission within the framework of the activities foreseen by the European Union Reference Laboratory for Avian Influenza and Newcastle Disease under grant agreement SI2.870510. This work was also partially supported by KAPPA-FLU HORIZON-CL6-2022-FARM2FORK-02-03 (grant agreement No 101084171) and FLU-SWITCH Era-Net ICRAD (grant agreement No 862605). ACB, AMPB and IHB were supported by the Biotechnology and Biological Sciences Research Council (BBSRC) and Department for Environment, Food and Rural Affairs (Defra, UK) research initiative ‘FluMAP’ [grant number BB/X006204/1]. Funding was also provided by Defra and the devolved administrations of Scotland and Wales through SE2213, SV3032 and SV3400. The authors wish to thank Francesca Ellero, Joe James and Caroline Bröjer for their careful revision of the manuscript. We gratefully acknowledge also the authors, originating and submitting laboratories of the sequences from GISAID’s EpiFlu™ Database on which this research is based in part (Supplementary Table S4).

PY - 2024/4/6

Y1 - 2024/4/6

N2 - Since 2016, A(H5Nx) high pathogenic avian influenza (HPAI) virus of clade 2.3.4.4b has become one of the most serious global threats not only to wild and domestic birds, but also to public health. In recent years, important changes in the ecology, epidemiology, and evolution of this virus have been reported, with an unprecedented global diffusion and variety of affected birds and mammalian species. After the two consecutive and devastating epidemic waves in Europe in 2020-2021 and 2021-2022, with the second one recognized as one of the largest epidemics recorded so far, this clade has begun to circulate endemically in European wild bird populations. This study used the complete genomes of 1,956 European HPAI A(H5Nx) viruses to investigate the virus evolution during this varying epidemiological outline. We investigated the spatiotemporal patterns of A(H5Nx) virus diffusion to/from and within Europe during the 2020-2021 and 2021-2022 epidemic waves, providing evidence of ongoing changes in transmission dynamics and disease epidemiology. We demonstrated the high genetic diversity of the circulating viruses, which have undergone frequent reassortment events, providing for the first time a complete overview and a proposed nomenclature of the multiple genotypes circulating in Europe in 2020-2022. We described the emergence of a new genotype with gull adapted genes, which offered the virus the opportunity to occupy new ecological niches, driving the disease endemicity in the European wild bird population. The high propensity of the virus for reassortment, its jumps to a progressively wider number of host species, including mammals, and the rapid acquisition of adaptive mutations make the trend of virus evolution and spread difficult to predict in this unfailing evolving scenario.

AB - Since 2016, A(H5Nx) high pathogenic avian influenza (HPAI) virus of clade 2.3.4.4b has become one of the most serious global threats not only to wild and domestic birds, but also to public health. In recent years, important changes in the ecology, epidemiology, and evolution of this virus have been reported, with an unprecedented global diffusion and variety of affected birds and mammalian species. After the two consecutive and devastating epidemic waves in Europe in 2020-2021 and 2021-2022, with the second one recognized as one of the largest epidemics recorded so far, this clade has begun to circulate endemically in European wild bird populations. This study used the complete genomes of 1,956 European HPAI A(H5Nx) viruses to investigate the virus evolution during this varying epidemiological outline. We investigated the spatiotemporal patterns of A(H5Nx) virus diffusion to/from and within Europe during the 2020-2021 and 2021-2022 epidemic waves, providing evidence of ongoing changes in transmission dynamics and disease epidemiology. We demonstrated the high genetic diversity of the circulating viruses, which have undergone frequent reassortment events, providing for the first time a complete overview and a proposed nomenclature of the multiple genotypes circulating in Europe in 2020-2022. We described the emergence of a new genotype with gull adapted genes, which offered the virus the opportunity to occupy new ecological niches, driving the disease endemicity in the European wild bird population. The high propensity of the virus for reassortment, its jumps to a progressively wider number of host species, including mammals, and the rapid acquisition of adaptive mutations make the trend of virus evolution and spread difficult to predict in this unfailing evolving scenario.

KW - Europe

KW - high pathogenic avian influenza A(H5) viruses

KW - phylodynamics

KW - reassortments

KW - spatial spread

UR - http://www.scopus.com/inward/record.url?scp=85192920841&partnerID=8YFLogxK

UR - https://pubmed.ncbi.nlm.nih.gov/38699215

U2 - 10.1093/ve/veae027

DO - 10.1093/ve/veae027

M3 - Article

C2 - 38699215

SN - 2057-1577

VL - 10

JO - Virus Evolution

JF - Virus Evolution

IS - 1

M1 - veae027

ER -

High pathogenic avian influenza A(H5) viruses of clade 2.3.4.4b in Europe - Why trends of virus evolution are more difficult to predict

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