1887
  1. Home
  2. Eurosurveillance
  3. Volume 30, Issue 22, 05/Jun/2025
  4. Article
Surveillance Open Access
Like 0
Download

Abstract

Background

Swine influenza has a considerable impact on pig populations and poses a pandemic threat to humans. However, little is known about the influenza A viruses circulating among pigs in the Netherlands.

Aim

We piloted a surveillance programme aimed at enabling swine influenza A virus (swIAV) surveillance in the Netherlands: investigated prevalence, genomic characteristics and recent evolution of circulating swIAV variants and compared them with relevant human and swine influenza viruses from the Netherlands and other European countries.

Methods

We collected and tested respiratory samples from pigs (2019–2023) for swIAV, characterised the viruses with molecular and virological methods and shared molecular data of swine and relevant human influenza A viruses in a national platform.

Results

We detected swIAV throughout the year in 342 (42%) of 824 respiratory samples from 90 farms. Complete genome sequencing identified 73 H1N1, 51 H1N2 and one H3N2 viruses. Phylogenetic analyses identified viruses from each of the three H1 swine lineages (1A/B/C) and four subclades. Viruses from the 1A lineage clustered into three subgroups with distinct antigenic properties, which seemed descendent from separate introductions of human seasonal A(H1N1)pdm09 viruses. Phenotypically, no reduced susceptibility to existing antiviral drugs oseltamivir and zanamivir was found.

Conclusion

We provided insights into swIAVs in pigs in the Netherlands, including antiviral susceptibility and antigenic differences. It highlighted occasional virus transmission between humans and pigs. Sharing swIAV data at a national level will be continued to reduce influenza burden in swine and support identification and characterisation of emerging swIAVs with zoonotic potential.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2025.30.22.2400664
2025-06-05
2025-06-29
/content/10.2807/1560-7917.ES.2025.30.22.2400664
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/30/22/eurosurv-30-22-2.html?itemId=/content/10.2807/1560-7917.ES.2025.30.22.2400664&mimeType=html&fmt=ahah

References

  1. Simon G, Larsen LE, Dürrwald R, Foni E, Harder T, Van Reeth K, et al. European surveillance network for influenza in pigs: surveillance programs, diagnostic tools and Swine influenza virus subtypes identified in 14 European countries from 2010 to 2013. PLoS One. 2014;9(12):e115815.  https://doi.org/10.1371/journal.pone.0115815  PMID: 25542013 
  2. Cogdale J, Kele B, Myers R, Harvey R, Lofts A, Mikaiel T, et al. A case of swine influenza A(H1N2)v in England, November 2023. Euro Surveill. 2024;29(3):2400002.  https://doi.org/10.2807/1560-7917.ES.2024.29.3.2400002  PMID: 38240057 
  3. Hennig C, Graaf A, Petric PP, Graf L, Schwemmle M, Beer M, et al. Are pigs overestimated as a source of zoonotic influenza viruses? Porcine Health Manag. 2022;8(1):30.  https://doi.org/10.1186/s40813-022-00274-x  PMID: 35773676 
  4. Henritzi D, Petric PP, Lewis NS, Graaf A, Pessia A, Starick E, et al. Surveillance of European domestic pig populations identifies an emerging reservoir of potentially zoonotic swine influenza A viruses. Cell Host Microbe. 2020;28(4):614-627.e6.  https://doi.org/10.1016/j.chom.2020.07.006  PMID: 32721380 
  5. Bekedam H. Zoonosen in het vizier. [Zoonoses in focus]. The Hague: Government of the Netherlands; 30 Jun 2021. Dutch. Available from: https://www.rijksoverheid.nl/documenten/rapporten/2021/06/01/rapport-expertgroep-zoonosen
  6. Gu M, Chen K, Ge Z, Jiao J, Cai T, Liu S, et al. Zoonotic threat of G4 genotype Eurasian avian-like swine influenza A(H1N1) viruses, China, 2020. Emerg Infect Dis. 2022;28(8):1664-8.  https://doi.org/10.3201/eid2808.212530  PMID: 35876682 
  7. Eggink D, Kroneman A, Dingemans J, Goderski G, van den Brink S, Bagheri M, et al. Human infections with Eurasian avian-like swine influenza virus detected by coincidence via routine respiratory surveillance systems, the Netherlands, 2020 to 2023. Euro Surveill. 2025;30(19):2400662.  https://doi.org/10.2807/1560-7917.ES.2025.30.19.2400662  PMID: 40376819 
  8. 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. PMID: 38116102 
  9. 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 
  10. Burrough ER, Magstadt DR, Petersen B, Timmermans SJ, Gauger PC, Zhang J, et al. Highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. Emerg Infect Dis. 2024;30(7):1335-43.  https://doi.org/10.3201/eid3007.240508  PMID: 38683888 
  11. Peacock TP, Moncla L, Dudas G, VanInsberghe D, Sukhova K, Lloyd-Smith JO, et al. The global H5N1 influenza panzootic in mammals. Nature. 2025;637(8045):304-13.  https://doi.org/10.1038/s41586-024-08054-z  PMID: 39317240 
  12. Munster VJ, Baas C, Lexmond P, Bestebroer TM, Guldemeester J, Beyer WEP, et al. Practical considerations for high-throughput influenza A virus surveillance studies of wild birds by use of molecular diagnostic tests. J Clin Microbiol. 2009;47(3):666-73.  https://doi.org/10.1128/JCM.01625-08  PMID: 19109483 
  13. King J, Harder T, Beer M, Pohlmann A. Rapid multiplex MinION nanopore sequencing workflow for Influenza A viruses. BMC Infect Dis. 2020;20(1):648.  https://doi.org/10.1186/s12879-020-05367-y  PMID: 32883215 
  14. Zwagemaker F, Hajji K, Schmitz D, Kroneman A. The RIVM-IDS Bioinformatics team. ViroConstrictor (Version 1.4.2). Available from:  https://doi.org/10.5281/zenodo.7688035 
  15. Beerens N, Heutink R, Bergervoet SA, Harders F, Bossers A, Koch G. Multiple reassorted viruses as cause of highly pathogenic avian influenza A(H5N8) virus epidemic, the Netherlands, 2016. Emerg Infect Dis. 2017;23(12):1974-81.  https://doi.org/10.3201/eid2312.171062  PMID: 29148396 
  16. Chang J, Anderson TK, Zeller MA, Gauger PC, Vincent AL. octoFLU: automated classification for the evolutionary origin of influenza A virus gene sequences detected in U.S. swine. Microbiol Resour Announc. 2019;8(32):e00673-19.  https://doi.org/10.1128/MRA.00673-19  PMID: 31395641 
  17. Olson RD, Assaf R, Brettin T, Conrad N, Cucinell C, Davis JJ, et al. Introducing the Bacterial and Viral Bioinformatics Resource Center (BV-BRC): a resource combining PATRIC, IRD and ViPR. Nucleic Acids Res. 2023;51(D1):D678-89.  https://doi.org/10.1093/nar/gkac1003  PMID: 36350631 
  18. 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 
  19. 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 
  20. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059-66.  https://doi.org/10.1093/nar/gkf436  PMID: 12136088 
  21. 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 
  22. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37(5):1530-4.  https://doi.org/10.1093/molbev/msaa015  PMID: 32011700 
  23. A*STAR Bioinformatics Institute (BII). Fluserver: Realtime monitoring of influenza mutations. Singapore: BII. [Accessed: 3 Jun 2025]. Available from: https://flusurver.bii.a-star.edu.sg/
  24. Jonges M, van der Lubben IM, Dijkstra F, Verhoef L, Koopmans M, Meijer A. Dynamics of antiviral-resistant influenza viruses in the Netherlands, 2005-2008. Antiviral Res. 2009;83(3):290-7.  https://doi.org/10.1016/j.antiviral.2009.07.003  PMID: 19591877 
  25. de Jong JC, Smith DJ, Lapedes AS, Donatelli I, Campitelli L, Barigazzi G, et al. Antigenic and genetic evolution of swine influenza A (H3N2) viruses in Europe. J Virol. 2007;81(8):4315-22.  https://doi.org/10.1128/JVI.02458-06  PMID: 17287258 
  26. Statistics Netherlands (CBS). Slightly smaller pig herd, barely reduced cattle herd. The Hague: CBS; 1 Oct 2021. Available from: https://www.cbs.nl/en-gb/news/2021/39/slightly-smaller-pig-herd-barely-reduced-cattle-herd
  27. Anderson TK, Macken CA, Lewis NS, Scheuermann RH, Van Reeth K, Brown IH, et al. A phylogeny-based global nomenclature system and automated annotation tool for H1 hemagglutinin genes from swine influenza A viruses. MSphere. 2016;1(6):e00275-16.  https://doi.org/10.1128/mSphere.00275-16  PMID: 27981236 
  28. Perez-Sautu U, Pozo F, Cuesta I, Monzon S, Calderon A, Gonzalez M, et al. Y155H amino acid substitution in influenza A(H1N1)pdm09 viruses does not confer a phenotype of reduced susceptibility to neuraminidase inhibitors. Euro Surveill. 2014;19(27):14-20.  https://doi.org/10.2807/1560-7917.ES2014.19.27.20849  PMID: 25033052 
  29. Parys A, Vereecke N, Vandoorn E, Theuns S, Van Reeth K. Surveillance and genomic characterization of influenza A and D viruses in swine, Belgium and the Netherlands, 2019-2021. Emerg Infect Dis. 2023;29(7):1459-64.  https://doi.org/10.3201/eid2907.221499  PMID: 37347825 
  30. Ryt-Hansen P, George S, Hjulsager CK, Trebbien R, Krog JS, Ciucani MM, et al. Rapid surge of reassortant A(H1N1) influenza viruses in Danish swine and their zoonotic potential. Emerg Microbes Infect. 2025;14(1):2466686.  https://doi.org/10.1080/22221751.2025.2466686  PMID: 39945729 
Swine influenza virus surveillance programme pilot to assess the risk for animal and public health, the Netherlands, 2022 to 2023
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Erhard+van+der+Vries&option1=author&noRedirect=true" class="nonDisambigAuthorLink">van der Vries Erhard</a>, <a href="/search?value1=Evelien+A+Germeraad&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Germeraad Evelien A</a>, <a href="/search?value1=Annelies+Kroneman&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kroneman Annelies</a>, <a href="/search?value1=Luc%C3%ADa+Dieste-P%C3%A9rez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Dieste-Pérez Lucía</a>, <a href="/search?value1=Dirk+Eggink&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Eggink Dirk</a>, <a href="/search?value1=Eveline+Willems&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Willems Eveline</a>, <a href="/search?value1=Alexander+MP+Byrne&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Byrne Alexander MP</a>, <a href="/search?value1=Nicola+Lewis&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lewis Nicola</a>, <a href="/search?value1=Manon+Houben&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Houben Manon</a>, <a href="/search?value1=Ron+Fouchier&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fouchier Ron</a>, <a href="/search?value1=Adam+Meijer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Meijer Adam</a>, <a href="/search?value1=Joke+van+der+Giessen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">van der Giessen Joke</a></span>. Swine influenza virus surveillance programme pilot to assess the risk for animal and public health, the Netherlands, 2022 to 2023. <a href="/content/ecdc">Euro Surveill.</a> 2025;30(22):pii=2400664. <a href="https://doi.org/10.2807/1560-7917.ES.2025.30.22.2400664" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2025.30.22.2400664</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 03 Oct 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 26 Mar 2025 </span> </p>
/content/10.2807/1560-7917.ES.2025.30.22.2400664
/content/10.2807/1560-7917.ES.2025.30.22.2400664
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error