1887
  1. Home
  2. Eurosurveillance
  3. Volume 30, Issue 23, 12/Jun/2025
  4. Article
Research Open Access
Like 0
Download

Abstract

Introduction

Influenza A(H1N1)pdm09, A(H3N2) and B/Victoria viruses circulated in Europe in 2023/24, with A(H1N1)pdm09 dominance. First influenza infections in childhood may lead to different vaccine effectiveness (VE) in subsequent years.

Aim

The VEBIS primary care network estimated influenza VE in Europe using a multicentre test‐negative study.

Methods

Primary care practitioners collected information and specimens from patients consulting with acute respiratory infection. We estimated VE against influenza (sub)type and clade, by age group and by year of age for A(H1N1)pdm09, using logistic regression.

Results

We included 29,958 patients, with 3,054, 1,053 and 311 influenza A(H1N1)pdm09, A(H3N2) and B cases, respectively. All-age VE against influenza A(H1N1)pdm09 was 52% (95% CI: 44–59). By year of age, VE was 27% (95% CI: −2 to 47) at 44 years with peaks at 72% (95% CI: 52–84) and 54% (95% CI: 41–64) among children and those 65 years and older, respectively. All-age A(H1N1)pdm09 VE against clade 5a.2a was 41% (95% CI: 24–54) and −11% (95% CI: −69 to 26) against clade 5a.2a.1. The A(H3N2) VE was 35% (95% CI: 20–48) among all ages and ranged between 34% and 40% by age group. All-age VE against clade 2a.3a.1 was 38% (95% CI: 1–62). All-age VE against B/Victoria was 83% (95% CI: 65–94), ranging between 70 and 92% by age group.

Discussion

The 2023/24 VEBIS primary care VE against medically attended symptomatic influenza infection was high against influenza B/Victoria, but lower against influenza A(H1N1)pdm09 and A(H3N2). Clade- and age-specific effects may have played a role in the lower A(H1N1)pdm09 VE.

© 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.2025.30.23.2500011
2025-06-12
2025-07-16
/content/10.2807/1560-7917.ES.2025.30.23.2500011
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/30/23/eurosurv-30-23-2.html?itemId=/content/10.2807/1560-7917.ES.2025.30.23.2500011&mimeType=html&fmt=ahah

References

  1. World Health Organization (WHO) Recommended composition of influenza virus vaccines for use in the 2023-2024 northern hemisphere influenza season. Geneva: WHO; 2023. Available from: https://www.who.int/publications/m/item/recommended-composition-of-influenza-virus-vaccines-for-use-in-the-2023-2024-northern-hemisphere-influenza-season
  2. European Centre for Disease Prevention and Control (ECDC). European Respiratory Virus Surveillance Summary (ERVISS). Stockholm: ECDC. [Accessed: 25 Jun 2024]. Available from: https://erviss.org
  3. Davenport FM, Hennessy AV, Francis T Jr. Epidemiologic and immunologic significance of age distribution of antibody to antigenic variants of influenza virus. J Exp Med. 1953;98(6):641-56.  https://doi.org/10.1084/jem.98.6.641  PMID: 13109114 
  4. Lewnard JA, Cobey S. Immune history and influenza vaccine effectiveness. Vaccines (Basel). 2018;6(2):28.  https://doi.org/10.3390/vaccines6020028  PMID: 29883414 
  5. Kelvin AA, Zambon M. Influenza imprinting in childhood and the influence on vaccine response later in life. Euro Surveill. 2019;24(48):1900720.  https://doi.org/10.2807/1560-7917.ES.2019.24.48.1900720  PMID: 31796156 
  6. Budd AP, Beacham L, Smith CB, Garten RJ, Reed C, Kniss K, et al. Birth cohort effects in influenza surveillance data: evidence that first influenza infection affects later influenza-associated illness. J Infect Dis. 2019;220(5):820-9.  https://doi.org/10.1093/infdis/jiz201  PMID: 31053844 
  7. Linderman SL, Chambers BS, Zost SJ, Parkhouse K, Li Y, Herrmann C, et al. Potential antigenic explanation for atypical H1N1 infections among middle-aged adults during the 2013-2014 influenza season. Proc Natl Acad Sci USA. 2014;111(44):15798-803.  https://doi.org/10.1073/pnas.1409171111  PMID: 25331901 
  8. Skowronski DM, Chambers C, Sabaiduc S, De Serres G, Winter AL, Dickinson JA, et al. Beyond antigenic match: possible agent-host and immuno-epidemiological influences on influenza vaccine effectiveness during the 2015-2016 season in Canada. J Infect Dis. 2017;216(12):1487-500.  https://doi.org/10.1093/infdis/jix526  PMID: 29029166 
  9. Flannery B, Smith C, Garten RJ, Levine MZ, Chung JR, Jackson ML, et al. Influence of birth cohort on effectiveness of 2015-2016 influenza vaccine against medically attended illness due to 2009 pandemic influenza A(H1N1) virus in the United States. J Infect Dis. 2018;218(2):189-96.  https://doi.org/10.1093/infdis/jix634  PMID: 29361005 
  10. Kissling E, Pozo F, Buda S, Vilcu AM, Rizzo C, Gherasim A, et al. Effectiveness of influenza vaccine against influenza A in Europe in seasons of different A(H1N1)pdm09 and the same A(H3N2) vaccine components (2016-17 and 2017-18). Vaccine X. 2019;3:100042.  https://doi.org/10.1016/j.jvacx.2019.100042  PMID: 31660536 
  11. Kissling E, Valenciano M, Falcao J, Larrauri A, Widgren K, Pitigoi D, et al. "I-MOVE" towards monitoring seasonal and pandemic influenza vaccine effectiveness: lessons learnt from a pilot multi-centric case-control study in Europe, 2008-9. Euro Surveill. 2009;14(44):19388.  https://doi.org/10.2807/ese.14.44.19388-en  PMID: 19941774 
  12. Valenciano M, Kissling E, Cohen JM, Oroszi B, Barret AS, Rizzo C, et al. Estimates of pandemic influenza vaccine effectiveness in Europe, 2009-2010: results of Influenza Monitoring Vaccine Effectiveness in Europe (I-MOVE) multicentre case-control study. PLoS Med. 2011;8(1):e1000388.  https://doi.org/10.1371/journal.pmed.1000388  PMID: 21379316 
  13. Kissling E, Valenciano M, Cohen JM, Oroszi B, Barret AS, Rizzo C, et al. I-MOVE multi-centre case control study 2010-11: overall and stratified estimates of influenza vaccine effectiveness in Europe. PLoS One. 2011;6(11):e27622. . Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3216983/ https://doi.org/10.1371/journal.pone.0027622  PMID: 22110695 
  14. Kissling E, Valenciano M, Buchholz U, Larrauri A, Cohen JM, Nunes B, et al. Influenza vaccine effectiveness estimates in Europe in a season with three influenza type/subtypes circulating: the I-MOVE multicentre case-control study, influenza season 2012/13. Euro Surveill. 2014;19(6):20701.  https://doi.org/10.2807/1560-7917.ES2014.19.6.20701  PMID: 24556348 
  15. Kissling E, Valenciano M, Pozo F, Vilcu AM, Reuss A, Rizzo C, et al. 2015/16 I-MOVE/I-MOVE+ multicentre case-control study in Europe: Moderate vaccine effectiveness estimates against influenza A(H1N1)pdm09 and low estimates against lineage-mismatched influenza B among children. Influenza Other Respir Viruses. 2018;12(4):423-37.  https://doi.org/10.1111/irv.12520  PMID: 29125681 
  16. Maurel M, Pozo F, Pérez-Gimeno G, Buda S, Sève N, Oroszi B, et al. Influenza vaccine effectiveness in Europe: Results from the 2022-2023 VEBIS (Vaccine Effectiveness, Burden and Impact Studies) primary care multicentre study. Influenza Other Respir Viruses. 2024;18(1):e13243.  https://doi.org/10.1111/irv.13243  PMID: 38204584 
  17. Ministerio de Sanidad. Actualización recomendaciones de vacunación estacional 2023-2024 en España. [Update on seasonal vaccination recommendations for 2023-2024 in Spain]. Madrid: Ministerio de Sanindad; 2023. Spanish. Available from: https://www.sanidad.gob.es/areas/promocionPrevencion/vacunaciones/programasDeVacunacion/docs/Recomendaciones_vacunacion_gripe.pdf
  18. Health Service Executive (HSE).. Getting the flu vaccine. Dublin: HSE. [Accessed: 25 Jun 2024]. Available from: https://www2.hse.ie/conditions/flu/get-vaccine
  19. Kissling E. Birth cohort-specific vaccine effectiveness against influenza A(H1N1)pdm09 in seasons with different A(H1N1)pdm09 virus vaccine components, I-MOVE multicentre primary care study, Europe, 2013/14 to 2018/19. Options X for the Control of Influenza; 29 Aug 2019, Singapore. Abstract 11047. Available from: https://isirv.org/site/images/conferences/Optionsx/optionsx_FA_a4_v7.pdf
  20. European Centre for Disease Prevention and Control (ECDC), Kissling E, Lanièce Delaunay C, Maurel M, Moren A, Nardone A. et al. Core protocol for ECDC studies of vaccine effectiveness against symptomatic laboratory-confirmed influenza or SARS-CoV-2 infection at primary care level: version 1.0. Stockholm, ECDC; 2023. Available from: https://data.europa.eu/doi/10.2900/25966
  21. European Commission. Communication from the Commission to the European Parliament, the Council, the European Economic and Social Committee and the Committee of the Regions on enabling the digital transformation of health and care in the Digital Single Market; empowering citizens and building a healthier society. Brussels: European Commission. 25 Apr 2018. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=celex:52018DC0233
  22. Liu M, Zhao X, Hua S, Du X, Peng Y, Li X, et al. Antigenic patterns and evolution of the human influenza A (H1N1) virus. Sci Rep. 2015;5(1):14171.  https://doi.org/10.1038/srep14171  PMID: 26412348 
  23. Harrell FE. Regression modeling strategies. With applications to linear models, logistic regression, and survival analysis. New York: Springer; 2001. Available from: http://link.springer.com/10.1007/978-1-4757-3462-1
  24. European Centre for Disease Prevention and Control (ECDC). Influenza virus characterisation: Summary report Europe, May 2024. Stockholm: ECDC; 2024. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/TD-6189-E_Euro-report_May24_final.pdf
  25. Skowronski DM, Zhan Y, Kaweski SE, Sabaiduc S, Khalid A, Olsha R, et al. 2023/24 mid-season influenza and Omicron XBB.1.5 vaccine effectiveness estimates from the Canadian Sentinel Practitioner Surveillance Network (SPSN). Euro Surveill. 2024;29(7):2400076.  https://doi.org/10.2807/1560-7917.ES.2024.29.7.2400076  PMID: 38362622 
  26. Whitaker H, Findlay B, Zitha J, Goudie R, Hassell K, Evans J, et al. Interim 2023/2024 season influenza vaccine effectiveness in primary and secondary care in the United Kingdom. Influenza Other Respir Viruses. 2024;18(5):e13284.  https://doi.org/10.1111/irv.13284  PMID: 38773753 
  27. Chung JR, Price AM, Zimmerman RK, Moehling Geffel K, House SL, Curley T, et al. Influenza vaccine effectiveness against medically attended outpatient illness, United States, 2023-24 season. Clin Infect Dis. 2025;ciae658.  https://doi.org/10.1093/cid/ciae658  PMID: 39761230 
  28. Kissling E, Pozo F, Martínez-Baz I, Buda S, Vilcu AM, Domegan L, et al. Influenza vaccine effectiveness against influenza A subtypes in Europe: Results from the 2021-2022 I-MOVE primary care multicentre study. Influenza Other Respir Viruses. 2023;17(1):e13069.  https://doi.org/10.1111/irv.13069  PMID: 36702797 
  29. Influenza virus characterization - Summary Europe, March 2024. 2024 [cited 2024 Jul 17]. Available from: https://www.ecdc.europa.eu/en/publications-data/influenza-virus-characterization-summary-europe-march-2024
  30. Liu STH, Behzadi MA, Sun W, Freyn AW, Liu WC, Broecker F, et al. Antigenic sites in influenza H1 hemagglutinin display species-specific immunodominance. J Clin Invest. 2018;128(11):4992-6.  https://doi.org/10.1172/JCI122895  PMID: 30188868 
  31. Skowronski DM, Sabaiduc S, Leir S, Rose C, Zou M, Murti M, et al. Paradoxical clade- and age-specific vaccine effectiveness during the 2018/19 influenza A(H3N2) epidemic in Canada: potential imprint-regulated effect of vaccine (I-REV). Euro Surveill. 2019;24(46):1900585.  https://doi.org/10.2807/1560-7917.ES.2019.24.46.1900585  PMID: 31771709 
  32. Kissling E, Pozo F, Buda S, Vilcu AM, Gherasim A, Brytting M, et al. Low 2018/19 vaccine effectiveness against influenza A(H3N2) among 15-64-year-olds in Europe: exploration by birth cohort. Euro Surveill. 2019;24(48):1900604.  https://doi.org/10.2807/1560-7917.ES.2019.24.48.1900604  PMID: 31796152 
  33. Frutos AM, Price AM, Harker E, Reeves EL, Ahmad HM, Murugan V, et al. Interim estimates of 2023-24 seasonal influenza vaccine effectiveness — United States. MMWR Morb Mortal Wkly Rep. 2024;73(8):168-74.  https://doi.org/10.15585/mmwr.mm7308a3 
  34. World Health Organization (WHO). Recommended composition of influenza virus vaccines for use in the 2024-2025 northern hemisphere influenza season. Geneva: WHO; 2024. Available from: https://cdn.who.int/media/docs/default-source/influenza/who-influenza-recommendations/vcm-northern-hemisphere-recommendation-2024-2025/recommended-composition-of-influenza-virus-vaccines-for-use-in-the-2024-2025-northern-hemisphere-influenza-season.pdf?sfvrsn=2e9d2194_7&download=true
  35. Skowronski DM, Chambers C, De Serres G, Sabaiduc S, Winter AL, Dickinson JA, et al. Serial vaccination and the antigenic distance hypothesis: effects on influenza vaccine effectiveness during A(H3N2) epidemics in Canada, 2010-2011 to 2014-2015. J Infect Dis. 2017;215(7):1059-99.  https://doi.org/10.1093/infdis/jix074  PMID: 28180277 
Influenza vaccine effectiveness in Europe and the birth cohort effect against influenza A(H1N1)pdm09: VEBIS primary care multicentre study, 2023/24
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Esther+Kissling&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kissling Esther</a>, <a href="/search?value1=Marine+Maurel&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Maurel Marine</a>, <a href="/search?value1=Francisco+Pozo&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pozo Francisco</a>, <a href="/search?value1=Gloria+P%C3%A9rez-Gimeno&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pérez-Gimeno Gloria</a>, <a href="/search?value1=Silke+Buda&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Buda Silke</a>, <a href="/search?value1=No%C3%A9mie+S%C3%A8ve&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sève Noémie</a>, <a href="/search?value1=Lisa+Domegan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Domegan Lisa</a>, <a href="/search?value1=Mari%C3%ABtte+Hooiveld&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Hooiveld Mariëtte</a>, <a href="/search?value1=Beatrix+Oroszi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Oroszi Beatrix</a>, <a href="/search?value1=Iv%C3%A1n+Mart%C3%ADnez-Baz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Martínez-Baz Iván</a>, <a href="/search?value1=Raquel+Guiomar&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Guiomar Raquel</a>, <a href="/search?value1=Neus+Latorre-Margalef&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Latorre-Margalef Neus</a>, <a href="/search?value1=Ivan+Mlinari%C4%87&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mlinarić Ivan</a>, <a href="/search?value1=Mihaela+Lazar&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lazar Mihaela</a>, <a href="/search?value1=Jaume+Gim%C3%A9nez+Duran&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Giménez Duran Jaume</a>, <a href="/search?value1=Ralf+D%C3%BCrrwald&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Dürrwald Ralf</a>, <a href="/search?value1=Vincent+Enouf&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Enouf Vincent</a>, <a href="/search?value1=Adele+McKenna&option1=author&noRedirect=true" class="nonDisambigAuthorLink">McKenna Adele</a>, <a href="/search?value1=Marit+de+Lange&option1=author&noRedirect=true" class="nonDisambigAuthorLink">de Lange Marit</a>, <a href="/search?value1=Gerg%C5%91+T%C3%BAri&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Túri Gergő</a>, <a href="/search?value1=Camino+Trobajo-Sanmart%C3%ADn&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Trobajo-Sanmartín Camino</a>, <a href="/search?value1=Ver%C3%B3nica+Gomez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gomez Verónica</a>, <a href="/search?value1=Tove+Samuelsson+Hagey&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Samuelsson Hagey Tove</a>, <a href="/search?value1=Vesna+Vi%C5%A1ekruna+Vu%C4%8Dina&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Višekruna Vučina Vesna</a>, <a href="/search?value1=Maria+Carmen+Cherciu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cherciu Maria Carmen</a>, <a href="/search?value1=Miriam+Garc%C3%ADa+Vazquez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">García Vazquez Miriam</a>, <a href="/search?value1=Annika+Erdwiens&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Erdwiens Annika</a>, <a href="/search?value1=Shirley+Masse&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Masse Shirley</a>, <a href="/search?value1=Charlene+Bennett&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bennett Charlene</a>, <a href="/search?value1=Adam+Meijer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Meijer Adam</a>, <a href="/search?value1=Katalin+Krist%C3%B3f&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kristóf Katalin</a>, <a href="/search?value1=Jes%C3%BAs+Castilla&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Castilla Jesús</a>, <a href="/search?value1=Ana+Paula+Rodrigues&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rodrigues Ana Paula</a>, <a href="/search?value1=Sanja+Kure%C4%8Di%C4%87+Filipovi%C4%87&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kurečić Filipović Sanja</a>, <a href="/search?value1=Alina+Elena+Ivanciuc&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ivanciuc Alina Elena</a>, <a href="/search?value1=Sabrina+Bacci&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bacci Sabrina</a>, <a href="/search?value1=Marlena+Kaczmarek&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kaczmarek Marlena</a>, <a href="/search?value1=on+behalf+of+the+European+primary+care+VE+group&option1=author&noRedirect=true" class="nonDisambigAuthorLink">on behalf of the European primary care VE group</a></span>. Influenza vaccine effectiveness in Europe and the birth cohort effect against influenza A(H1N1)pdm09: VEBIS primary care multicentre study, 2023/24. <a href="/content/ecdc">Euro Surveill.</a> 2025;30(23):pii=2500011. <a href="https://doi.org/10.2807/1560-7917.ES.2025.30.23.2500011" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2025.30.23.2500011</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 23 Dec 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 07 Apr 2025 </span> </p>
/content/10.2807/1560-7917.ES.2025.30.23.2500011
/content/10.2807/1560-7917.ES.2025.30.23.2500011
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