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Abstract

Highly pathogenic avian influenza (HPAI) has caused widespread mortality in both wild and domestic birds in Europe 2020–2023. In July 2023, HPAI A(H5N1) was detected on 27 fur farms in Finland. In total, infections in silver and blue foxes, American minks and raccoon dogs were confirmed by RT-PCR. The pathological findings in the animals include widespread inflammatory lesions in the lungs, brain and liver, indicating efficient systemic dissemination of the virus. Phylogenetic analysis of Finnish A(H5N1) strains from fur animals and wild birds has identified three clusters (Finland I-III), and molecular analyses revealed emergence of mutations known to facilitate viral adaptation to mammals in the PB2 and NA proteins. Findings of avian influenza in fur animals were spatially and temporally connected with mass mortalities in wild birds. The mechanisms of virus transmission within and between farms have not been conclusively identified, but several different routes relating to limited biosecurity on the farms are implicated. The outbreak was managed in close collaboration between animal and human health authorities to mitigate and monitor the impact for both animal and human health.

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/content/10.2807/1560-7917.ES.2024.29.25.2400063
2024-06-20
2024-07-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.25.2400063
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References

  1. Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness. Wkly Epidemiol Rec. 2018;93(12):142-52. PMID: 29569430 
  2. Floyd T, Banyard AC, Lean FZX, Byrne AMP, Fullick E, Whittard E, et al. Encephalitis and death in wild mammals at a rehabilitation center after infection with highly pathogenic avian influenza A(H5N8) virus, United Kingdom. Emerg Infect Dis. 2021;27(11):2856-63.  https://doi.org/10.3201/eid2711.211225  PMID: 34670647 
  3. Rijks JM, Hesselink H, Lollinga P, Wesselman R, Prins P, Weesendorp E, et al. Highly pathogenic avian influenza A(H5N1) virus in wild red foxes, the Netherlands, 2021. Emerg Infect Dis. 2021;27(11):2960-2.  https://doi.org/10.3201/eid2711.211281  PMID: 34670656 
  4. European Food Safety AuthorityEuropean Centre for Disease Prevention and ControlEuropean Union Reference Laboratory for Avian InfluenzaAdlhoch C, Fusaro A, Gonzales JL, et al. Avian influenza overview September-December 2023. EFSA J. 2023;21(12):e8539.  https://doi.org/10.2903/j.efsa.2023.8539  PMID: 38116102 
  5. Tammiranta N, Isomursu M, Fusaro A, Nylund M, Nokireki T, Giussani E, et al. Highly pathogenic avian influenza A (H5N1) virus infections in wild carnivores connected to mass mortalities of pheasants in Finland. Infect Genet Evol. 2023;111:105423.  https://doi.org/10.1016/j.meegid.2023.105423  PMID: 36889484 
  6. Agüero M, Monne I, Sánchez A, Zecchin B, Fusaro A, Ruano MJ, et al. Highly pathogenic avian influenza A(H5N1) virus infection in farmed minks, Spain, October 2022. Euro Surveill. 2023;28(3):2300001.  https://doi.org/10.2807/1560-7917.ES.2023.28.3.2300001  PMID: 36695488 
  7. The Finnish Food Authority (FFA). Eläintautien valvonta- ja seurantaohjelmat 2023, versio 2. [Surveillance and monitoring programmes of animal diseases 2023, version 2]. Helsinki: FFA. [Accessed: 2 Apr 2024]. Available from: https://www.ruokavirasto.fi/globalassets/elaimet/elainten-terveys-ja-elaintaudit/elaintautien-seuranta--ja-valvontaohjelmat-2023_2.pdf
  8. Lindh E, Lounela H, Ikonen N, Kantala T, Savolainen-Kopra C, Kauppinen A, et al. Highly pathogenic avian influenza A(H5N1) virus infection on multiple fur farms in the South and Central Ostrobothnia regions of Finland, July 2023. Euro Surveill. 2023;28(31):2300400.  https://doi.org/10.2807/1560-7917.ES.2023.28.31.2300400  PMID: 37535475 
  9. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772-80.  https://doi.org/10.1093/molbev/mst010  PMID: 23329690 
  10. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol Biol Evol. 2018;35(2):518-22.  https://doi.org/10.1093/molbev/msx281  PMID: 29077904 
  11. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587-9.  https://doi.org/10.1038/nmeth.4285  PMID: 28481363 
  12. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268-74.  https://doi.org/10.1093/molbev/msu300  PMID: 25371430 
  13. Fusaro A, Zecchin B, Giussani E, Palumbo E, Agüero-García M, Bachofen C, et al. 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 Evol. 2024;10(1):veae027.  https://doi.org/10.1093/ve/veae027  PMID: 38699215 
  14. Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16(1):37-48.  https://doi.org/10.1093/oxfordjournals.molbev.a026036  PMID: 10331250 
  15. Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 2018;4(1):vey016.  https://doi.org/10.1093/ve/vey016  PMID: 29942656 
  16. Shapiro B, Rambaut A, Drummond AJ. Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol. 2006;23(1):7-9.  https://doi.org/10.1093/molbev/msj021  PMID: 16177232 
  17. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol. 2012;29(9):2157-67.  https://doi.org/10.1093/molbev/mss084  PMID: 22403239 
  18. Minin VN, Bloomquist EW, Suchard MA. Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol Biol Evol. 2008;25(7):1459-71.  https://doi.org/10.1093/molbev/msn090  PMID: 18408232 
  19. Minin VN, Suchard MA. Counting labeled transitions in continuous-time Markov models of evolution. J Math Biol. 2008;56(3):391-412.  https://doi.org/10.1007/s00285-007-0120-8  PMID: 17874105 
  20. Lemey P, Rambaut A, Drummond AJ, Suchard MA. Bayesian phylogeography finds its roots. PLOS Comput Biol. 2009;5(9):e1000520.  https://doi.org/10.1371/journal.pcbi.1000520  PMID: 19779555 
  21. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7(1):214.  https://doi.org/10.1186/1471-2148-7-214  PMID: 17996036 
  22. Shapiro B, Ho SY, Drummond AJ, Suchard MA, Pybus OG, Rambaut A. A Bayesian phylogenetic method to estimate unknown sequence ages. Mol Biol Evol. 2011;28(2):879-87.  https://doi.org/10.1093/molbev/msq262  PMID: 20889726 
  23. Suchard MA, Rambaut A. Many-core algorithms for statistical phylogenetics. Bioinformatics. 2009;25(11):1370-6.  https://doi.org/10.1093/bioinformatics/btp244  PMID: 19369496 
  24. Bielejec F, Baele G, Vrancken B, Suchard MA, Rambaut A, Lemey P. SpreaD3: Interactive visualization of spatiotemporal history and trait evolutionary processes. Mol Biol Evol. 2016;33(8):2167-9.  https://doi.org/10.1093/molbev/msw082  PMID: 27189542 
  25. Rossow H, Seppä-Lassila L, Joutsen S, Järvelä T, Tuominen P. Zoonoses on fur farms – risk profile. Finnish Food Authority Research Reports 4/2023. Helsinki: Finnish Food Authority; 2023. Available from: http://hdl.handle.net/10138/564730
  26. Bussey KA, Bousse TL, Desmet EA, Kim B, Takimoto T. PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J Virol. 2010;84(9):4395-406.  https://doi.org/10.1128/JVI.02642-09  PMID: 20181719 
  27. Zhang H, Li X, Guo J, Li L, Chang C, Li Y, et al. The PB2 E627K mutation contributes to the high polymerase activity and enhanced replication of H7N9 influenza virus. J Gen Virol. 2014;95(Pt 4):779-86.  https://doi.org/10.1099/vir.0.061721-0  PMID: 24394699 
  28. Subbarao EK, London W, Murphy BR. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol. 1993;67(4):1761-4.  https://doi.org/10.1128/jvi.67.4.1761-1764.1993  PMID: 8445709 
  29. Salomon R, Franks J, Govorkova EA, Ilyushina NA, Yen H-L, Hulse-Post DJ, et al. The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J Exp Med. 2006;203(3):689-97.  https://doi.org/10.1084/jem.20051938  PMID: 16533883 
  30. Steel J, Lowen AC, Mubareka S, Palese P. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 2009;5(1):e1000252.  https://doi.org/10.1371/journal.ppat.1000252  PMID: 19119420 
  31. Du W, Guo H, Nijman VS, Doedt J, van der Vries E, van der Lee J, et al. The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance. PLoS Pathog. 2019;15(6):e1007860.  https://doi.org/10.1371/journal.ppat.1007860  PMID: 31181126 
  32. Du W, de Vries E, van Kuppeveld FJM, Matrosovich M, de Haan CAM. Second sialic acid-binding site of influenza A virus neuraminidase: binding receptors for efficient release. FEBS J. 2021;288(19):5598-612.  https://doi.org/10.1111/febs.15668  PMID: 33314755 
  33. Danzy S, Studdard LR, Manicassamy B, Solorzano A, Marshall N, García-Sastre A, et al. Mutations to PB2 and NP proteins of an avian influenza virus combine to confer efficient growth in primary human respiratory cells. J Virol. 2014;88(22):13436-46.  https://doi.org/10.1128/JVI.01093-14  PMID: 25210184 
  34. Fan S, Hatta M, Kim JH, Halfmann P, Imai M, Macken CA, et al. Novel residues in avian influenza virus PB2 protein affect virulence in mammalian hosts. Nat Commun. 2014;5(1):5021.  https://doi.org/10.1038/ncomms6021  PMID: 25289523 
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