1887
  1. Home
  2. Eurosurveillance
  3. Volume 29, Issue 8, 22/Feb/2024
  4. Article
Research Open Access
Like 0
Download

Abstract

Background

Waning immunity from seasonal influenza vaccination can cause suboptimal protection during peak influenza activity. However, vaccine effectiveness studies assessing waning immunity using vaccinated and unvaccinated individuals are subject to biases.

Aim

We examined the association between time since vaccination and laboratory-confirmed influenza to assess the change in influenza vaccine protection over time.

Methods

Using linked laboratory and health administrative databases in Ontario, Canada, we identified community-dwelling individuals aged ≥ 6 months who received an influenza vaccine before being tested for influenza by RT-PCR during the 2010/11 to 2018/19 influenza seasons. We estimated the adjusted odds ratio (aOR) for laboratory-confirmed influenza by time since vaccination (categorised into intervals) and for every 28 days.

Results

There were 53,065 individuals who were vaccinated before testing for influenza, with 10,264 (19%) influenza-positive cases. The odds of influenza increased from 1.05 (95% CI: 0.91–1.22) at 42–69 days after vaccination and peaked at 1.27 (95% CI: 1.04–1.55) at 126–153 days when compared with the reference interval (14–41 days). This corresponded to 1.09-times increased odds of influenza every 28 days (aOR = 1.09; 95% CI: 1.04–1.15). Individuals aged 18–64 years showed the greatest decline in protection against influenza A(H1N1) (aOR = 1.26; 95% CI: 0.97–1.64), whereas for individuals aged ≥ 65 years, it was against influenza A(H3N2) (aOR = 1.20; 95% CI: 1.08–1.33). We did not observe evidence of waning vaccine protection for individuals aged < 18 years.

Conclusions

Influenza vaccine protection wanes during an influenza season. Understanding the optimal timing of vaccination could ensure robust protection during seasonal influenza activity.

© 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.2024.29.8.2300239
2024-02-22
2024-11-21
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.8.2300239
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/8/eurosurv-29-8-4.html?itemId=/content/10.2807/1560-7917.ES.2024.29.8.2300239&mimeType=html&fmt=ahah

References

  1. Skowronski DM, Tweed SA, De Serres G. Rapid decline of influenza vaccine-induced antibody in the elderly: is it real, or is it relevant? J Infect Dis. 2008;197(4):490-502.  https://doi.org/10.1086/524146  PMID: 18275271 
  2. Petrie JG, Ohmit SE, Johnson E, Truscon R, Monto AS. Persistence of antibodies to influenza hemagglutinin and neuraminidase following one or two years of influenza vaccination. J Infect Dis. 2015;212(12):1914-22.  https://doi.org/10.1093/infdis/jiv313  PMID: 26014800 
  3. Mordant FL, Price OH, Rudraraju R, Slavin MA, Marshall C, Worth LJ, et al. Antibody titres elicited by the 2018 seasonal inactivated influenza vaccine decline by 3 months post-vaccination but persist for at least 6 months. Influenza Other Respir Viruses. 2023;17(1):e13072.  https://doi.org/10.1111/irv.13072  PMID: 36451293 
  4. Ferdinands JM, Alyanak E, Reed C, Fry AM. Waning of influenza vaccine protection: exploring the trade-offs of changes in vaccination timing among older adults. Clin Infect Dis. 2020;70(8):1550-9.  https://doi.org/10.1093/cid/ciz452  PMID: 31257422 
  5. Young B, Sadarangani S, Jiang L, Wilder-Smith A, Chen MIC. Duration of influenza vaccine effectiveness: a systematic review, meta-analysis, and meta-regression of test-negative design case-control studies. J Infect Dis. 2018;217(5):731-41.  https://doi.org/10.1093/infdis/jix632  PMID: 29220496 
  6. Lipsitch M. Challenges of vaccine effectiveness and waning studies. Clin Infect Dis. 2019;68(10):1631-3.  https://doi.org/10.1093/cid/ciy773  PMID: 30204853 
  7. Lipsitch M, Goldstein E, Ray GT, Fireman B. Depletion-of-susceptibles bias in influenza vaccine waning studies: how to ensure robust results. Epidemiol Infect. 2019;147:e306.  https://doi.org/10.1017/S0950268819001961  PMID: 31774051 
  8. Young BE, Mak TM, Ang LW, Sadarangani S, Ho HJ, Wilder-Smith A, et al. Influenza vaccine failure in the tropics: a retrospective cohort study of waning effectiveness. Epidemiol Infect. 2020;148:e299.  https://doi.org/10.1017/S0950268820002952  PMID: 33261680 
  9. Ray GT, Lewis N, Klein NP, Daley MF, Wang SV, Kulldorff M, et al. Intraseason waning of influenza vaccine effectiveness. Clin Infect Dis. 2019;68(10):1623-30.  https://doi.org/10.1093/cid/ciy770  PMID: 30204855 
  10. Kwong JC, Buchan SA, Chung H, Campitelli MA, Schwartz KL, Crowcroft NS, et al. Can routinely collected laboratory and health administrative data be used to assess influenza vaccine effectiveness? Assessing the validity of the Flu and Other Respiratory Viruses Research (FOREVER) Cohort. Vaccine. 2019;37(31):4392-400.  https://doi.org/10.1016/j.vaccine.2019.06.011  PMID: 31221563 
  11. Sinilaite A, Papenburg J on behalf of the National Advisory Committee on Immunization (NACI). Summary of the National Advisory Committee on Immunization (NACI) Seasonal Influenza Vaccine Statement for 2022-2023. Can Commun Dis Rep. 2022;48(9):373-82.  https://doi.org/10.14745/ccdr.v48i09a01 
  12. Buchan SA, Chung H, Campitelli MA, Crowcroft NS, Gubbay JB, Karnauchow T, et al. Vaccine effectiveness against laboratory-confirmed influenza hospitalizations among young children during the 2010-11 to 2013-14 influenza seasons in Ontario, Canada. PLoS One. 2017;12(11):e0187834.  https://doi.org/10.1371/journal.pone.0187834  PMID: 29149183 
  13. Liu H. Cochran-Armitage Trend Test Using SAS n.d. Lex Jansen. [Accessed: 6 Nov 2023]. Available from: https://www.lexjansen.com/pharmasug/2007/sp/SP05.pdf
  14. Fang J, Austin PC, Tu JV. Test for linearity between continuous confounder and binary outcome first, run a multivariate regression analysis second. SAS Glob Forum [serial online]. 2009;252-2009. Available from: https://www.researchgate.net/publication/228827696_Test_for_linearity_between_continuous_confounder_and_binary_outcome_first_run_a_multivariate_regression_analysis_second
  15. SAS Help Center. Testing linear hypotheses about the regression coefficients. Cary: SAS. [Accessed: 6 Nov 2023]. Available from: https://documentation.sas.com/doc/en/pgmsascdc/9.4_3.3/statug/statug_logistic_details36.htm
  16. Belongia EA, Sundaram ME, McClure DL, Meece JK, Ferdinands J, VanWormer JJ. Waning vaccine protection against influenza A (H3N2) illness in children and older adults during a single season. Vaccine. 2015;33(1):246-51.  https://doi.org/10.1016/j.vaccine.2014.06.052  PMID: 24962752 
  17. Doyon-Plourde P, Przepiorkowski J, Young K, Zhao L, Sinilaite A. Intraseasonal waning immunity of seasonal influenza vaccine - A systematic review and meta-analysis. Vaccine. 2023;41(31):4462-71.  https://doi.org/10.1016/j.vaccine.2023.06.038  PMID: 37331840 
  18. Sahni LC, Naioti EA, Olson SM, Campbell AP, Michaels MG, Williams JV, et al. Sustained within-season vaccine effectiveness against influenza-associated hospitalization in children: evidence from the New Vaccine Surveillance Network, 2015-2016 through 2019-2020. Clin Infect Dis. 2023;76(3):e1031-9.  https://doi.org/10.1093/cid/ciac577  PMID: 35867698 
  19. Black S, Nicolay U, Vesikari T, Knuf M, Del Giudice G, Della Cioppa G, et al. Hemagglutination inhibition antibody titers as a correlate of protection for inactivated influenza vaccines in children. Pediatr Infect Dis J. 2011;30(12):1081-5.  https://doi.org/10.1097/INF.0b013e3182367662  PMID: 21983214 
  20. Seidman JC, Richard SA, Viboud C, Miller MA. Quantitative review of antibody response to inactivated seasonal influenza vaccines. Influenza Other Respir Viruses. 2012;6(1):52-62.  https://doi.org/10.1111/j.1750-2659.2011.00268.x  PMID: 21668661 
  21. Fisman DN, Savage R, Gubbay J, Achonu C, Akwar H, Farrell DJ, et al. Older age and a reduced likelihood of 2009 H1N1 virus infection. N Engl J Med. 2009;361(20):2000-1.  https://doi.org/10.1056/NEJMc0907256  PMID: 19907052 
  22. Miller MS, Gardner TJ, Krammer F, Aguado LC, Tortorella D, Basler CF, et al. Neutralizing antibodies against previously encountered influenza virus strains increase over time: a longitudinal analysis. Sci Transl Med. 2013;5(198):198ra107.  https://doi.org/10.1126/scitranslmed.3006637  PMID: 23946196 
  23. Skowronski DM, Chambers C, Sabaiduc S, De Serres G, Winter AL, Dickinson JA, et al. A Perfect storm: impact of genomic variation and serial vaccination on low influenza vaccine effectiveness during the 2014-2015 season. Clin Infect Dis. 2016;63(1):21-32.  https://doi.org/10.1093/cid/ciw176  PMID: 27025838 
  24. Skowronski DM, Janjua NZ, De Serres G, Sabaiduc S, Eshaghi A, Dickinson JA, et al. Low 2012-13 influenza vaccine effectiveness associated with mutation in the egg-adapted H3N2 vaccine strain not antigenic drift in circulating viruses. PLoS One. 2014;9(3):e92153.  https://doi.org/10.1371/journal.pone.0092153  PMID: 24667168 
  25. Skowronski DM, Chambers C, De Serres G, Sabaiduc S, Winter AL, Dickinson JA, et al. Vaccine effectiveness against lineage-matched and -mismatched influenza B viruses across 8 seasons in Canada, 2010-2011 to 2017-2018. Clin Infect Dis. 2019;68(10):1754-7.  https://doi.org/10.1093/cid/ciy876  PMID: 30312364 
  26. Carrat F, Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine. 2007;25(39-40):6852-62.  https://doi.org/10.1016/j.vaccine.2007.07.027  PMID: 17719149 
  27. Schwartz KL, Jembere N, Campitelli MA, Buchan SA, Chung H, Kwong JC. Using physician billing claims from the Ontario Health Insurance Plan to determine individual influenza vaccination status: an updated validation study. CMAJ Open. 2016;4(3):E463-70.  https://doi.org/10.9778/cmajo.20160009  PMID: 27730110 
Measuring waning protection from seasonal influenza vaccination during nine influenza seasons, Ontario, Canada, 2010/11 to 2018/19
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Hannah+Chung&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chung Hannah</a>, <a href="/search?value1=Michael+A+Campitelli&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Campitelli Michael A</a>, <a href="/search?value1=Sarah+A+Buchan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Buchan Sarah A</a>, <a href="/search?value1=Aaron+Campigotto&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Campigotto Aaron</a>, <a href="/search?value1=Natasha+S+Crowcroft&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Crowcroft Natasha S</a>, <a href="/search?value1=Jonathan+B+Gubbay&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gubbay Jonathan B</a>, <a href="/search?value1=James+KH+Jung&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jung James KH</a>, <a href="/search?value1=Timothy+Karnauchow&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Karnauchow Timothy</a>, <a href="/search?value1=Kevin+Katz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Katz Kevin</a>, <a href="/search?value1=Allison+J+McGeer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">McGeer Allison J</a>, <a href="/search?value1=J+Dayre+McNally&option1=author&noRedirect=true" class="nonDisambigAuthorLink">McNally J Dayre</a>, <a href="/search?value1=David+C+Richardson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Richardson David C</a>, <a href="/search?value1=Susan+E+Richardson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Richardson Susan E</a>, <a href="/search?value1=Laura+C+Rosella&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rosella Laura C</a>, <a href="/search?value1=Margaret+L+Russell&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Russell Margaret L</a>, <a href="/search?value1=Kevin+L+Schwartz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Schwartz Kevin L</a>, <a href="/search?value1=Andrew+Simor&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Simor Andrew</a>, <a href="/search?value1=Marek+Smieja&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Smieja Marek</a>, <a href="/search?value1=Maria+E+Sundaram&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sundaram Maria E</a>, <a href="/search?value1=Bryna+F+Warshawsky&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Warshawsky Bryna F</a>, <a href="/search?value1=George+Zahariadis&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Zahariadis George</a>, <a href="/search?value1=Jeffrey+C+Kwong&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kwong Jeffrey C</a>, <a href="/search?value1=on+behalf+of+the+Canadian+Immunization+Research+Network+%28CIRN%29+Provincial+Collaborative+Network+%28PCN%29+Investigators&option1=author&noRedirect=true" class="nonDisambigAuthorLink">on behalf of the Canadian Immunization Research Network (CIRN) Provincial Collaborative Network (PCN) Investigators</a></span>. Measuring waning protection from seasonal influenza vaccination during nine influenza seasons, Ontario, Canada, 2010/11 to 2018/19. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(8):pii=2300239. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.8.2300239" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.8.2300239</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 29 Apr 2023;&nbsp;&nbsp; <span class="generated">Accepted</span>: 29 Nov 2023 </span> </p>
/content/10.2807/1560-7917.ES.2024.29.8.2300239
/content/10.2807/1560-7917.ES.2024.29.8.2300239
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