538
Views
0
CrossRef citations to date
0
Altmetric
Original Research

Waning intra-season vaccine effectiveness against influenza A(H3N2) underlines the need for more durable protection

, ORCID Icon, , , , , , & show all
Pages 380-388 | Received 11 Jan 2024, Accepted 12 Mar 2024, Published online: 18 Mar 2024

References

  • World Health Organization (WHO). Vaccines against influenza: WHO position paper – May 2022. Wkly Epidemiol Rec. 2022;97(19):185–208.
  • Sellers SA, Hagan RS, Hayden FG, et al. The hidden burden of influenza: a review of the extra-pulmonary complications of influenza infection. Influenza Other Respir Viruses. 2017;11(5):372–393. doi: 10.1111/irv.12470
  • Centers for Disease Control and Prevention (CDC). Past seasons’ vaccine effectiveness estimates. [cited 2023 Nov 15]. Available from: https://www.cdc.gov/flu/vaccines-work/past-seasons-estimates.html
  • Domnich A, Manini I, Calabrò GE, et al. Mapping host-related correlates of influenza vaccine-induced immune response: an umbrella review of the available systematic reviews and meta-analyses. Vaccines (Basel). 2019;7(4):215. doi: 10.3390/vaccines7040215
  • Belongia EA, Simpson MD, King JP, et al. Variable influenza vaccine effectiveness by subtype: a systematic review and meta-analysis of test-negative design studies. Lancet Infect Dis. 2016;16(8):942–951. doi: 10.1016/s1473-3099(16)00129-8
  • Domnich A, Manini I, Panatto D, et al. Immunogenicity measures of influenza vaccines: a study of 1164 registered clinical trials. Vaccines (Basel). 2020;8(2):325. doi: 10.3390/vaccines8020325
  • Wen S, Wu Z, Zhong S, et al. Factors influencing the immunogenicity of influenza vaccines. Hum Vaccin Immunother. 2021;17(8):2706–2718. doi: 10.1080/21645515.2021.1875761
  • Rastogi S, Gross PA, Bonelli J, et al. Time to peak serum antibody response to influenza vaccine. Clin Diagn Lab Immunol. 1995;2(1):120–121. doi: 10.1128/cdli.2.1.120-121.1995
  • Kositanont U, Assantachai P, Wasi C, et al. Kinetics of the antibody response to seasonal influenza vaccination among the elderly. Viral Immunol. 2012;25(6):471–476. doi: 10.1089/vim.2012.0024
  • Doyon-Plourde P, Przepiorkowski J, Young K, et al. Intraseasonal waning immunity of seasonal influenza vaccine – a systematic review and meta-analysis. Vaccine. 2023;41(31):4462–4471.
  • Hoa LNM, Sullivan SG, Mai LQ, et al. Influenza A(H1N1)pdm09 but not A(H3N2) virus infection induces durable seroprotection: results from the ha nam cohort. J Infect Dis. 2022;226(1):59–69. doi: 10.1093/infdis/jiaa293
  • Carlock MA, Ingram JG, Clutter EF, et al. Impact of age and pre-existing immunity on the induction of human antibody responses against influenza B viruses. Hum Vaccin Immunother. 2019;15(9):2030–2043. doi: 10.1080/21645515.2019.1642056
  • Gilbert PB, Fong Y, Juraska M, et al. HAI and NAI titer correlates of inactivated and live attenuated influenza vaccine efficacy. BMC Infect Dis. 2019;19(1):453. doi: 10.1186/s12879-019-4049-5
  • Ferdinands JM, Fry AM, Reynolds S, et al. Intraseason waning of influenza vaccine protection: evidence from the US influenza vaccine effectiveness network, 2011–12 through 2014–15. Clin Infect Dis. 2017;64(5):544–550.
  • Ferdinands JM, Gaglani M, Martin ET, et al. Waning vaccine effectiveness against influenza-associated hospitalizations among adults, 2015–2016 to 2018–2019, United States Hospitalized Adult Influenza Vaccine Effectiveness Network. Clin Infect Dis. 2021;73(4):726–729.
  • Hu W, Sjoberg PA, Fries AC, et al. Waning vaccine protection against influenza among department of defense adult beneficiaries in the United States, 2016–2017 through 2019–2020 influenza seasons. Vaccines (Basel). 2022;10(6):888.
  • Young B, Sadarangani S, Jiang L, et al. 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):731–741. doi: 10.1093/infdis/jix632
  • Radin JM, Hawksworth AW, Myers CA, et al. Influenza vaccine effectiveness: maintained protection throughout the duration of influenza seasons 2010-2011 through 2013–2014. Vaccine. 2016;34(33):3907–3912.
  • Petrie JG, Ohmit SE, Truscon R, et al. Modest waning of influenza vaccine efficacy and antibody titers during the 2007–2008 influenza season. J Infect Dis. 2016;214(8):1142–1149.
  • Kissling E, Nunes B, Robertson C, et al. I-MOVE multicentre case-control study 2010/11 to 2014/15: is there within-season waning of influenza type/subtype vaccine effectiveness with increasing time since vaccination? Euro Surveill. 2016;21(16). doi: 10.2807/1560-7917.es.2016.21.16.30201
  • Lipsitch M, Goldstein E, Ray GT, et al. Depletion-of-susceptibles bias in influenza vaccine waning studies: how to ensure robust results. Epidemiol Infect. 2019;147:e306. doi: 10.1017/S0950268819001961
  • Ray GT, Lewis N, Klein NP, et al. Intraseason waning of influenza vaccine effectiveness. Clin Infect Dis. 2019;68(10):1623–1630. doi: 10.1093/cid/ciy770
  • Chung H, Campitelli MA, Buchan SA, et al. Measuring waning protection from seasonal influenza vaccination during nine influenza seasons, Ontario, Canada, 2010/11 to 2018/19. Euro Surveill. 2024;29(8). doi: 10.2807/1560-7917.ES.2024.29.8.2300239.
  • Costantino V, Trent M, MacIntyre CR. Modelling of optimal timing for influenza vaccination as a function of intraseasonal waning of immunity and vaccine coverage. Vaccine. 2019;37(44):6768–6775. doi: 10.1016/j.vaccine.2019.08.069.
  • Newall AT, Chen C, Wood JG, et al. Within-season influenza vaccine waning suggests potential net benefits to delayed vaccination in older adults in the United States. Vaccine. 2018;36(39):5910–5915. doi: 10.1016/j.vaccine.2018.08.007.
  • DRIVE consortium. Core protocol for type/brand specific influenza vaccine effectiveness studies (test-negative design studies). [cited 2023 Nov 15]. Available from: https://www.drive-eu.org/index.php/results/deliverables/
  • Domnich A, Orsi A, Ogliastro M, et al. Influenza vaccine effectiveness in preventing hospital encounters for laboratory-confirmed infection among Italian adults, 2022/23 season. Vaccine. 2023;41(33):4861–4866. doi: 10.1016/j.vaccine.2023.06.072
  • Rizzo C, Gesualdo F, Loconsole D, et al. Moderate vaccine effectiveness against severe acute respiratory infection caused by A(H1N1)pdm09 influenza virus and no effectiveness against A(H3N2) influenza virus in the 2018/2019 season in Italy. Vaccines (Basel). 2020;8(3):427.
  • Panatto D, Domnich A, Chironna M, et al. Surveillance of severe acute respiratory infection and influenza vaccine effectiveness among hospitalized Italian adults, 2021/22 season. Vaccines (Basel). 2022;11(1):83. doi: 10.3390/vaccines11010083
  • Tenforde MW, Chung J, Smith ER, et al. Influenza vaccine effectiveness in inpatient and outpatient settings in the United States, 2015–2018. Clin Infect Dis. 2021;73(3):386–392.
  • Doll MK, Pettigrew SM, Ma J, et al. Effects of confounding bias in coronavirus disease 2019 (COVID-19) and influenza vaccine effectiveness test-negative designs due to correlated influenza and COVID-19 vaccination behaviors. Clin Infect Dis. 2022;75(1):e564–e571. doi: 10.1093/cid/ciac234
  • Puig-Barberà J, Mira-Iglesias A, Tortajada-Girbés M, et al. Waning protection of influenza vaccination during four influenza seasons, 2011/2012 to 2014/2015. Vaccine. 2017;35(43):5799–5807. doi: 10.1016/j.vaccine.2017.09.035
  • Belongia EA, Sundaram ME, McClure DL, et al. Waning vaccine protection against influenza a (H3N2) illness in children and older adults during a single season. Vaccine. 2015;33(1):246–251. doi: 10.1016/j.vaccine.2014.06.052
  • Belongia EA, McLean HQ. Influenza vaccine effectiveness: Defining the H3N2 problem. Clin Infect Dis. 2019;69(10):1817–1823. doi: 10.1093/cid/ciz411
  • Pando R, Stern S, Nemet I, et al. Diversity in the circulation of influenza A(H3N2) viruses in the Northern Hemisphere in the 2018-19 season. Vaccines (Basel). 2021;9(4):375.
  • Song JY, Cheong HJ, Hwang IS, et al. Long-term immunogenicity of influenza vaccine among the elderly: risk factors for poor immune response and persistence. Vaccine. 2010;28(23):3929–3935. doi: 10.1016/j.vaccine.2010.03.067
  • Cobey S, Gouma S, Parkhouse K, et al. Poor immunogenicity, not vaccine strain egg adaptation, may explain the low H3N2 influenza vaccine effectiveness in 2012–2013. Clin Infect Dis. 2018;67(3):327–333.
  • Jones-Gray E, Robinson EJ, Kucharski AJ, et al. Does repeated influenza vaccination attenuate effectiveness? A systematic review and meta-analysis. Lancet Respir Med. 2023;11(1):27–44. doi: 10.1016/S2213-2600(22)00266-1
  • Thompson MG, Naleway A, Fry AM, et al. Effects of repeated annual inactivated influenza vaccination among healthcare personnel on serum hemagglutinin inhibition antibody response to A/Perth/16/2009 (H3N2)-like virus during 2010–11. Vaccine. 2016;34(7):981–988. doi: 10.1016/j.vaccine.2015.10.119
  • Thompson MG, Cowling BJ. How repeated influenza vaccination effects might apply to COVID-19 vaccines. Lancet Respir Med. 2022;10(7):636–638. doi: 10.1016/S2213-2600(22)00162-X
  • Debbink K, McCrone JT, Petrie JG, et al. Vaccination has minimal impact on the intrahost diversity of H3N2 influenza viruses. PLoS Pathog. 2017;13(1):e1006194. doi: 10.1371/journal.ppat.1006194
  • Seidman JC, Richard SA, Viboud C, et al. Quantitative review of antibody response to inactivated seasonal influenza vaccines. Influenza Other Respir Viruses. 2012;6(1):52–62. doi: 10.1111/j.1750-2659.2011.00268.x
  • Sumner KM, Masalovich S, O’Halloran A, et al. Severity of influenza-associated hospitalisations by influenza virus type and subtype in the USA, 2010–19: a repeated cross-sectional study. Lancet Microbe. 2023;4(11):e903–e912.
  • Stuurman AL, Levi M, Beutels P, et al. Investigating confounding in network-based test-negative design influenza vaccine effectiveness studies-experience from the DRIVE project. Influenza Other Respir Viruses. 2023;17(1):e13087.
  • European Centres for Disease Prevention and Control (ECDC). Summary of the influenza 2016–2017 season in Europe. [cited 2023 Nov 15]. Available from: https://www.ecdc.europa.eu/en/publications-data/summary-influenza-2016-2017-season-europe#:~:text=The%20season%20lasted%20for%2027,%2F2016%20and%205%2F2017
  • European Centres for Disease Prevention and Control (ECDC). Seasonal influenza 2022−2023. Annual epidemiological report for 2023 [cited 2023 Nov 15]. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/seasonal-influenza-annual-epidemiological-report-2022-2023.pdf
  • Domnich A, Orsi A, Ogliastro M, et al. Exploring missed opportunities for influenza vaccination and influenza vaccine co-administration patterns among Italian older adults: a retrospective cohort study. Eur J Public Health. 2023;33(6):1183–1187. doi: 10.1093/eurpub/ckad155
  • Italian Ministry of Health. Prevention and control of influenza: recommendations for the 2023-24 season. [cited 2023 Nov 15]. Available from: https://www.trovanorme.salute.gov.it/norme/renderNormsanPdf?anno=2023&codLeg=93294&parte=1%20&serie=null
  • Williams KV, Krauland MG, Harrison LH, et al. Can a two-dose influenza vaccine regimen better protect older adults? An agent-based modeling study. Vaccines (Basel). 2022;10(11):1799. doi: 10.3390/vaccines10111799
  • Cordero E, Roca-Oporto C, Bulnes-Ramos A, et al. Two doses of inactivated influenza vaccine improve immune response in solid organ transplant recipients: Results of TRANSGRIPE 1–2, a randomized controlled clinical trial. Clin Infect Dis. 2017;64(7):829–838.
  • Ljungman P, Nahi H, Linde A. Vaccination of patients with haematological malignancies with one or two doses of influenza vaccine: a randomised study. Br J Haematol. 2005;130(1):96–98. doi: 10.1111/j.1365-2141.2005.05582.x
  • Nunes MC, Cutland CL, Moultrie A, et al. Immunogenicity and safety of different dosing schedules of trivalent inactivated influenza vaccine in pregnant women with HIV: a randomised controlled trial. Lancet HIV. 2020;7(2):e91–e103. doi: 10.1016/S2352-3018(19)30322-4
  • Domnich A, de Waure C. Comparative effectiveness of adjuvanted versus high-dose seasonal influenza vaccines for older adults: a systematic review and meta-analysis. Int J Infect Dis. 2022;122:855–863. doi: 10.1016/j.ijid.2022.07.048
  • Grohskopf LA, Blanton LH, Ferdinands JM, et al. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices—United States, 2023–24 influenza season. MMWR Recomm Rep. 2023;72(2):1–25. doi: 10.15585/mmwr.rr7202a1
  • Noh JY, Song JY, Choi WS, et al. Immunogenicity of trivalent influenza vaccines in patients with chronic kidney disease undergoing hemodialysis: MF59-adjuvanted versus non-adjuvanted vaccines. Hum Vaccin Immunother. 2016;12(11):2902–2908. doi: 10.1080/21645515.2016.1191717
  • Shartouny JR, Lowen AC. Message in a bottle: mRNA vaccination for influenza. J Gen Virol. 2022;103(7):001765. doi: 10.1099/jgv.0.001765
  • Shinde V, Cho I, Plested JS, et al. Comparison of the safety and immunogenicity of a novel matrix-M-adjuvanted nanoparticle influenza vaccine with a quadrivalent seasonal influenza vaccine in older adults: a phase 3 randomised controlled trial. Lancet Infect Dis. 2022;22(1):73–84. doi: 10.1016/s1473-3099(21)00192-4