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Volume 105, Issue 5

Iceland: an underestimated hub for the spread of high-pathogenicity avian influenza viruses in the North Atlantic Open Access

Abstract

High-pathogenicity avian influenza viruses (HPAIVs) of the goose/Guangdong lineage are enzootically circulating in wild bird populations worldwide. This increases the risk of entry into poultry production and spill-over to mammalian species, including humans. Better understanding of the ecological and epizootiological networks of these viruses is essential to optimize mitigation measures. Based on full genome sequences of 26 HPAIV samples from Iceland, which were collected between spring and autumn 2022, as well as 1 sample from the 2023 summer period, we show that 3 different genotypes of HPAIV H5N1 clade 2.3.4.4b were circulating within the wild bird population in Iceland in 2022. Furthermore, in 2023 we observed a novel introduction of HPAIV H5N5 of the same clade to Iceland. The data support the role of Iceland as an utmost northwestern distribution area in Europe that might act also as a potential bridging point for intercontinental spread of HPAIV across the North Atlantic.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): avian influenza , Iceland and wild birds
Funding
This study was supported by the:
  • Deutsche Forschungsgemeinschaft (Award 453012513)
    • Principle Award Recipient: AnnKathrin Ahrens
  • European Commission (Award 874735)
    • Principle Award Recipient: MartinBeer
  • HORIZON EUROPE Framework Programme (Award 101084171)
    • Principle Award Recipient: MartinBeer
  • Bundesministerium für Bildung und Forschung (Award 13N15449)
    • Principle Award Recipient: AnnePohlmann
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2024-05-02
2024-05-18
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References

  1. Barberis A, Boudaoud A, Gorrill A, Loupias J, Ghram A et al. Full-length genome sequences of the first H9N2 avian influenza viruses isolated in the Northeast of Algeria. Virol J 2020; 17:108 [View Article] [PubMed]
     [Google Scholar]
  2. Liang Y. Pathogenicity and virulence of influenza. Virulence 2023; 14:2223057 [View Article] [PubMed]
     [Google Scholar]
  3. Lu L, Lycett SJ, Leigh Brown AJ. Reassortment patterns of avian influenza virus internal segments among different subtypes. BMC Evol Biol 2014; 14:16 [View Article] [PubMed]
     [Google Scholar]
  4. Shao W, Li X, Goraya MU, Wang S, Chen J-L. Evolution of influenza A virus by mutation and re-assortment. Int J Mol Sci 2017; 18:1650 [View Article] [PubMed]
     [Google Scholar]
  5. Böttcher-Friebertshäuser E, Klenk HD, Garten W. Activation of influenza viruses by proteases from host cells and bacteria in the human airway epithelium. Pathog Dis 2013; 69:87–100 [View Article] [PubMed]
     [Google Scholar]
  6. Bertram S, Glowacka I, Steffen I, Kühl A, Pöhlmann S. Novel insights into proteolytic cleavage of influenza virus hemagglutinin. Rev Med Virol 2010; 20:298–310 [View Article] [PubMed]
     [Google Scholar]
  7. Lebarbenchon C, Chang C-M, van der Werf S, Aubin J-T, Kayser Y et al. Influenza A virus in birds during spring migration in the Camargue, France. J Wildl Dis 2007; 43:789–793 [View Article] [PubMed]
     [Google Scholar]
  8. Verhagen JH, Fouchier RAM, Lewis N. Highly pathogenic avian influenza viruses at the wild-domestic bird interface in Europe: future directions for research and surveillance. Viruses 2021; 13:212 [View Article] [PubMed]
     [Google Scholar]
  9. Hassan MM, Hoque MA, Debnath NC, Yamage M, Klaassen M. Are poultry or wild birds the main reservoirs for avian influenza in Bangladesh?. Ecohealth 2017; 14:490–500 [View Article] [PubMed]
     [Google Scholar]
  10. Shin D-L, Siebert U, Lakemeyer J, Grilo M, Pawliczka I et al. Highly pathogenic avian influenza A(H5N8) virus in gray seals, Baltic Sea. Emerg Infect Dis 2019; 25:2295–2298 [View Article] [PubMed]
     [Google Scholar]
  11. Claes F, Morzaria SP, Donis RO. Emergence and dissemination of clade 2.3.4.4 H5Nx influenza viruses-how is the Asian HPAI H5 lineage maintained. Curr Opin Virol 2016; 16:158–163 [View Article] [PubMed]
     [Google Scholar]
  12. Caliendo V, Lewis NS, Pohlmann A, Baillie SR, Banyard AC et al. Transatlantic spread of highly pathogenic avian influenza H5N1 by wild birds from Europe to North America in 2021. Sci Rep 2022; 12:11729 [View Article] [PubMed]
     [Google Scholar]
  13. Lycett SJ, Duchatel F, Digard P. A brief history of bird flu. Philos Trans R Soc Lond B Biol Sci 2019; 374:20180257 [View Article] [PubMed]
     [Google Scholar]
  14. Kandeil A, Patton C, Jones JC, Jeevan T, Harrington WN et al. Rapid evolution of A(H5N1) influenza viruses after intercontinental spread to North America. Nat Commun 2023; 14:3082 [View Article] [PubMed]
     [Google Scholar]
  15. Günther A, Krone O, Svansson V, Pohlmann A, King J et al. Iceland as stepping stone for spread of highly pathogenic avian influenza virus between Europe and North America. Emerg Infect Dis 2022; 28:2383–2388 [View Article] [PubMed]
     [Google Scholar]
  16. Harder TC, Teuffert J, Starick E, Gethmann J, Grund C et al. Highly pathogenic avian influenza virus (H5N1) in frozen duck carcasses, Germany, 2007. Emerg Infect Dis 2009; 15:272–279 [View Article] [PubMed]
     [Google Scholar]
  17. Hoffmann B, Hoffmann D, Henritzi D, Beer M, Harder TC. Riems influenza a typing array (RITA): an RT-qPCR-based low density array for subtyping avian and mammalian influenza a viruses. Sci Rep 2016; 6:27211 [View Article] [PubMed]
     [Google Scholar]
  18. Hassan KE, Ahrens AK, Ali A, El-Kady MF, Hafez HM et al. Improved subtyping of avian influenza viruses using an RT-qPCR-based low density array: “Riems Influenza a Typing Array”, Version 2 (RITA-2). Viruses 2022; 14:415 [View Article] [PubMed]
     [Google Scholar]
  19. King J, Harder T, Beer M, Pohlmann A. Rapid multiplex MinION nanopore sequencing workflow for Influenza A viruses. BMC Infect Dis 2020; 20:648 [View Article] [PubMed]
     [Google Scholar]
  20. King J, Harder T, Globig A, Stacker L, Günther A et al. Highly pathogenic avian influenza virus incursions of subtype H5N8, H5N5, H5N1, H5N4, and H5N3 in Germany during 2020-21. Virus Evol 2022; 8:veac035 [View Article] [PubMed]
     [Google Scholar]
  21. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  22. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
     [Google Scholar]
  23. Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 2009; 26:1641–1650 [View Article] [PubMed]
     [Google Scholar]
  24. Pohlmann A, Harder T. Genotype Differentiation of Highly Pathogenic Avian Influenza Viruses (HPAIV) of the Goose/Guangdong Lineage in Germany - Derivation and Deployment of Reference Sequences 2023
     [Google Scholar]
  25. Pohlmann A, King J, Fusaro A, Zecchin B, Banyard AC et al. Has epizootic become enzootic? Evidence for a fundamental change in the infection dynamics of highly pathogenic avian influenza in Europe, 2021. mBio 2022; 13:e0060922 [View Article] [PubMed]
     [Google Scholar]
  26. Yang Z, O’Brien JD, Zheng X, Zhu H-Q, She Z-S. Tree and rate estimation by local evaluation of heterochronous nucleotide data. Bioinformatics 2007; 23:169–176 [View Article] [PubMed]
     [Google Scholar]
  27. Alkie TN, Byrne AMP, Jones MEB, Mollett BC, Bourque L et al. Recurring trans-Atlantic incursion of clade 2.3.4.4b H5N1 viruses by long distance migratory birds from Northern Europe to Canada in 2022/2023. Viruses 2023; 15:1836 [View Article] [PubMed]
     [Google Scholar]
  28. Bergervoet SA, Ho CKY, Heutink R, Bossers A, Beerens N. Spread of highly pathogenic avian influenza (HPAI) H5N5 viruses in Europe in 2016-2017 appears related to the timing of reassortment events. Viruses 2019; 11:501 [View Article] [PubMed]
     [Google Scholar]
  29. Liang Y, Nissen JN, Krog JS, Breum SØ, Trebbien R et al. Novel clade 2.3.4.4b highly pathogenic avian influenza A H5N8 and H5N5 viruses in Denmark, 2020. Viruses 2021; 13:886 [View Article] [PubMed]
     [Google Scholar]
  30. Zinyakov N, Andriyasov A, Zhestkov P, Kozlov A, Nikonova Z et al. Analysis of avian influenza (H5N5) viruses isolated in the Southwestern European part of the Russian Federation in 2020-2021. Viruses 2022; 14:2725 [View Article] [PubMed]
     [Google Scholar]
  31. Adlhoch C, Fusaro A, Gonzales JL, Kuiken T, Mirinavičiūtė G et al. Avian influenza overview June-September 2023. EFSA J 2023; 21:e08328 [View Article] [PubMed]
     [Google Scholar]
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Iceland: an underestimated hub for the spread of high-pathogenicity avian influenza viruses in the North Atlantic
J. Gen. Virol. 105, 001985 (2024); https://doi.org/10.1099/jgv.0.001985
/content/journal/jgv/10.1099/jgv.0.001985
/content/journal/jgv/10.1099/jgv.0.001985
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