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Abstract

Introduction

Influenza A(H3N2) clades 3C.2a and 3C.3a co-circulated in Europe in 2018/19. Immunological imprinting by first childhood influenza infection may induce future birth cohort differences in vaccine effectiveness (VE).

Aim

The I-MOVE multicentre primary care test-negative study assessed 2018/19 influenza A(H3N2) VE by age and genetic subgroups to explore VE by birth cohort.

Methods

We measured VE against influenza A(H3N2) and (sub)clades. We stratified VE by usual age groups (0–14, 15–64, ≥ 65-years). To assess the imprint-regulated effect of vaccine (I-REV) hypothesis, we further stratified the middle-aged group, notably including 32–54-year-olds (1964–86) sharing potential childhood imprinting to serine at haemagglutinin position 159.

Results

Influenza A(H3N2) VE among all ages was −1% (95% confidence interval (CI): −24 to 18) and 46% (95% CI: 8–68), −26% (95% CI: −66 to 4) and 20% (95% CI: −20 to 46) among 0–14, 15–64 and ≥ 65-year-olds, respectively. Among 15–64-year-olds, VE against clades 3C.2a1b and 3C.3a was 15% (95% CI: −34 to 50) and −74% (95% CI: −259 to 16), respectively. VE was −18% (95% CI: −140 to 41), −53% (95% CI: −131 to −2) and −12% (95% CI: −74 to 28) among 15–31-year-olds (1987–2003), 32–54-year-olds (1964–86) and 55–64-year-olds (1954–63), respectively.

Discussion

The lowest 2018/19 influenza A(H3N2) VE was against clade 3C.3a and among those born 1964–86, corresponding to the I-REV hypothesis. The low influenza A(H3N2) VE in 15–64-year-olds and the public health impact of the I-REV hypothesis warrant further study.

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/content/10.2807/1560-7917.ES.2019.24.48.1900604
2019-11-28
2019-12-12
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.48.1900604
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References

  1. European Centre for Disease Prevention and Control (ECDC), World Health Organization Regional Office for Europe (WHO/Europe). Flu News Europe. Summary week 20/2019 (13-20 May 2019). 13-May-2019. Stockholm: ECDC; 2019. Available from: https://flunewseurope.org/Archives/GetFile?fileId=422
  2. World Health Organization (WHO). Addendum to the recommended composition of influenza virus vaccines for use in the 2019-2020 northern hemisphere influenza season. Geneva: WHO; 2019. Available from: https://www.who.int/influenza/vaccines/virus/recommendations/201902_recommendation_addendum.pdf?ua=1
  3. World Health Organization (WHO). Recommended composition of influenza virus vaccines for use in the 2018-2019 northern hemisphere influenza season. Geneva: WHO; 2018. Available from: https://www.who.int/influenza/vaccines/virus/recommendations/201802_recommendation.pdf?ua=1
  4. 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 
  5. 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 
  6. Kissling E, Rose A, Emborg HD, Gherasim A, Pebody R, Pozo F, et al. . Interim 2018/19 influenza vaccine effectiveness: six European studies, October 2018 to January 2019. Euro Surveill. 2019;24(8):1900121.  https://doi.org/10.2807/1560-7917.ES.2019.24.1900121  PMID: 30808440 
  7. 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 
  8. Flannery B, Kondor RJG, Chung JR, Gaglani M, Reis M, Zimmerman RK, et al. Spread of antigenically drifted influenza A(H3N2) viruses and vaccine effectiveness in the United States during the 2018-2019 season. J Infect Dis. 2019;jiz543.  https://doi.org/10.1093/infdis/jiz543  PMID: 31665373 
  9. Francis ME, King ML, Kelvin AA. Back to the future for influenza preimmunity-looking back at influenza virus history to infer the outcome of future infections. Viruses. 2019;11(2):122.  https://doi.org/10.3390/v11020122  PMID: 30704019 
  10. Davenport FM, Hennessy AV. Predetermination by infection and by vaccination of antibody response to influenza virus vaccines. J Exp Med. 1957;106(6):835-50.  https://doi.org/10.1084/jem.106.6.835  PMID: 13481247 
  11. Francis T. On the doctrine of original antigenic sin. Proc Am Philos Soc. 1960;104(6):572-8.
  12. Viboud C, Epstein SL. First flu is forever. Science. 2016;354(6313):706-7.  https://doi.org/10.1126/science.aak9816  PMID: 27846592 
  13. 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 
  14. Lewnard JA, Cobey S. Immune history and influenza vaccine effectiveness. Vaccines (Basel). 2018;6(2):28.  https://doi.org/10.3390/vaccines6020028  PMID: 29883414 
  15. Monto AS, Malosh RE, Petrie JG, Martin ET. The doctrine of original antigenic sin: separating good from evil. J Infect Dis. 2017;215(12):1782-8.  https://doi.org/10.1093/infdis/jix173  PMID: 28398521 
  16. Gostic KM, Ambrose M, Worobey M, Lloyd-Smith JO. Potent protection against H5N1 and H7N9 influenza via childhood hemagglutinin imprinting. Science. 2016;354(6313):722-6.  https://doi.org/10.1126/science.aag1322  PMID: 27846599 
  17. Shu Y, McCauley J. GISAID: Global initiative on sharing all influenza data - from vision to reality. Euro Surveill. 2017;22(13):30494.  https://doi.org/10.2807/1560-7917.ES.2017.22.13.30494  PMID: 28382917 
  18. Koel BF, Burke DF, Bestebroer TM, van der Vliet S, Zondag GC, Vervaet G, et al. Substitutions near the receptor binding site determine major antigenic change during influenza virus evolution. Science. 2013;342(6161):976-9.  https://doi.org/10.1126/science.1244730  PMID: 24264991 
  19. Klingen TR, Reimering S, Loers J, Mooren K, Klawonn F, Krey T, et al. Sweep Dynamics (SD) plots: Computational identification of selective sweeps to monitor the adaptation of influenza A viruses. Sci Rep. 2018;8(1):373.  https://doi.org/10.1038/s41598-017-18791-z  PMID: 29321538 
  20. Koel BF, Burke DF, van der Vliet S, Bestebroer TM, Rimmelzwaan GF, Osterhaus ADME, et al. Epistatic interactions can moderate the antigenic effect of substitutions in haemagglutinin of influenza H3N2 virus. J Gen Virol. 2019;100(5):773-7.  https://doi.org/10.1099/jgv.0.001263  PMID: 31017567 
  21. Valenciano M, Ciancio B, on behalf of the I-MOVE study team. I-MOVE: a European network to measure the effectiveness of influenza vaccines. Euro Surveill. 2012;17(39):20281.  https://doi.org/10.2807/ese.17.39.20281-en  PMID: 23041022 
  22. 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 
  23. Fukushima W, Hirota Y. Basic principles of test-negative design in evaluating influenza vaccine effectiveness. Vaccine. 2017;35(36):4796-800.  https://doi.org/10.1016/j.vaccine.2017.07.003  PMID: 28818471 
  24. European Commission. Commission Decision 2009/363/EC of 30 April 2009 amending Decision 2002/253/EC laying down case definitions for reporting communicable diseases to the Community network under Decision No 2119/98/EC of the European Parliament and of the Council. OJ L 110, 1.5.2009 p. 58. Available from: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2009:110:0058:0059:EN:PDF
  25. World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310(20):2191-4.  https://doi.org/10.1001/jama.2013.281053  PMID: 24141714 
  26. Kissling E, Valenciano M, Larrauri A, Oroszi B, Cohen JM, Nunes B, et al. Low and decreasing vaccine effectiveness against influenza A(H3) in 2011/12 among vaccination target groups in Europe: results from the I-MOVE multicentre case-control study. Euro Surveill. 2013;18(5):20390.  https://doi.org/10.2807/ese.18.05.20390-en  PMID: 23399425 
  27. 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 
  28. Valenciano M, Kissling E, Reuss A, Rizzo C, Gherasim A, Horváth JK, et al. . Vaccine effectiveness in preventing laboratory-confirmed influenza in primary care patients in a season of co-circulation of influenza A(H1N1)pdm09, B and drifted A(H3N2), I-MOVE Multicentre Case-Control Study, Europe 2014/15. Euro Surveill. 2016;21(7):30139.  https://doi.org/10.2807/1560-7917.ES.2016.21.7.30139  PMID: 26924024 
  29. Valenciano M, Kissling E, Reuss A, Jiménez-Jorge S, Horváth JK, Donnell JM, et al. . The European I-MOVE Multicentre 2013-2014 Case-Control Study. Homogeneous moderate influenza vaccine effectiveness against A(H1N1)pdm09 and heterogenous results by country against A(H3N2). Vaccine. 2015;33(24):2813-22.  https://doi.org/10.1016/j.vaccine.2015.04.012  PMID: 25936723 
  30. Advisory Committee on Immunization Practices (ACIP). Agency updates; influenza vaccines. Atlanta: Centers for Disease Control and Prevention; 27-Jun-2019. Available from: https://www.cdc.gov/vaccines/acip/meetings/live-mtg-2019-06.html
  31. European Centre for Disease Prevention and Control (ECDC). Influenza virus characterisation, Summary Europe, June 2019. Stockholm: ECDC; 2019. Available from: https://www.ecdc.europa.eu/en/publications-data/influenza-virus-characterisation-summary-europe-june-2019
  32. Linster M, Schrauwen EJA, van der Vliet S, Burke DF, Lexmond P, Bestebroer TM, et al. The molecular basis for antigenic drift of human A/H2N2 influenza viruses. J Virol. 2019;93(8):e01907-18.  https://doi.org/10.1128/JVI.01907-18  PMID: 30700609 
  33. Matsuzawa Y, Iwatsuki-Horimoto K, Nishimoto Y, Abe Y, Fukuyama S, Hamabata T, et al. Antigenic change in human influenza A(H2N2) viruses detected by using human plasma from aged and younger adult individuals. Viruses. 2019;11(11):978.  https://doi.org/10.3390/v11110978  PMID: 31652870 
  34. European Centre for Disease Prevention and Control (ECDC). Seasonal influenza vaccination and antiviral use in Europe. Overview of vaccination recommendations and coverage rates in the EU Member States for the 2013-14 and 2014-15 influenza seasons. Stockholm: ECDC; 2016. Available from: https://www.ecdc.europa.eu/sites/default/files/media/en/publications/Publications/Seasonal-influenza-vaccination-antiviral-use-europe.pdf
  35. Xie H, Li L, Ye Z, Li X, Plant EP, Zoueva O, et al. Differential effects of prior influenza exposures on H3N2 cross-reactivity of human postvaccination sera. Clin Infect Dis. 2017;65(2):259-67.  https://doi.org/10.1093/cid/cix269  PMID: 28369230 
  36. Butler D. Long-term studies will track indelible marks of first flu. Nature. 2019; Epub ahead of print.  PMID: 31118518 
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