2,266
Views
11
CrossRef citations to date
0
Altmetric
Review

Immunogenicity of influenza vaccine in elderly people: a systematic review and meta-analysis of randomized controlled trials, and its association with real-world effectiveness

, , , , , & ORCID Icon show all
Pages 2680-2689 | Received 09 Jan 2020, Accepted 23 Mar 2020, Published online: 29 Apr 2020

References

  • Iuliano AD, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, Cohen C, Gran JM, Schanzer D, Cowling BJ, et al. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet. 2018;391(10127):1285–300. doi:10.1016/S0140-6736(17)33293-2.
  • Nichols MK, Andrew MK, Hatchette TF, Ambrose A, Boivin G, Bowie W, Chit A, Dos Santos G, ElSherif M, Green K, et al. Influenza vaccine effectiveness to prevent influenza-related hospitalizations and serious outcomes in Canadian adults over the 2011/12 through 2013/14 influenza seasons: A pooled analysis from the Canadian Immunization Research Network (CIRN) Serious Outcomes Surveillance (SOS Network).. Vaccine. 2018;36(16):2166–75. doi:10.1016/j.vaccine.2018.02.093.
  • Andrew MK, Bowles SK, Pawelec G, Haynes L, Kuchel GA, McNeil SA, McElhaney JE. Influenza vaccination in older adults: recent innovations and practical applications. Drugs Aging. 2019;36(1):29–37. doi:10.1007/s40266-018-0597-4.
  • Tauraso NM, O’Brien TC, Seligman EJ. Problems of influenza virus vaccine standardization. Bull World Health Organ. 1969;41:497–506.
  • Skowronski DM, Gilbert M, Tweed SA, Petric M, Li Y, Mak A, McNabb G, De Serres G. Effectiveness of vaccine against medical consultation due to laboratory-confirmed influenza: results from a sentinel physician pilot project in British Columbia, 2004-2005. Can Commun Dis Rep. 2005;31(18):181–91.
  • Belongia EA, Simpson MD, King JP, Sundaram ME, Kelley NS, Osterholm MT, McLean HQ. Variable influenza vaccine effectiveness by subtype: a systematic review and meta-analysis of test-negative design studies. Lancet Infect Dis. 2016;16(8):942–51. doi:10.1016/S1473-3099(16)00129-8.
  • Darvishian M, van den Heuvel ER, Bissielo A, Castilla J, Cohen C, Englund H, Gefenaite G, Huang W-T, la Bastide-van Gemert S, Martinez-Baz I, et al. Effectiveness of seasonal influenza vaccination in community-dwelling elderly people: an individual participant data meta-analysis of test-negative design case-control studies. Lancet Respir Med. 2017;5(3):200–11. doi:10.1016/S2213-2600(17)30043-7.
  • Nair H, Brooks WA, Katz M, Roca A, Berkley JA, Madhi SA, Simmerman JM, Gordon A, Sato M, Howie S, et al. Global burden of respiratory infections due to seasonal influenza in young children: a systematic review and meta-analysis. Lancet. 2011;378(9807):1917–30. doi:10.1016/S0140-6736(11)61051-9.
  • Ohmit SE, Thompson MG, Petrie JG, Thaker SN, Jackson ML, Belongia EA, Zimmerman RK, Gaglani M, Lamerato L, Spencer SM, et al. Influenza vaccine effectiveness in the 2011-2012 season: protection against each circulating virus and the effect of prior vaccination on estimates. Clin Infect Dis. 2014;58(3):319–27. doi:10.1093/cid/cit736.
  • Russell K, Chung JR, Monto AS, Martin ET, Belongia EA, McLean HQ, Gaglani M, Murthy K, Zimmerman RK, Nowalk MP, et al. Influenza vaccine effectiveness in older adults compared with younger adults over five seasons. Vaccine. 2018;36(10):1272–78. doi:10.1016/j.vaccine.2018.01.045.
  • Dominguez A, Soldevila N, Toledo D, Godoy P, Espejo E, Fernandez MA, Mayoral JM, Castilla J, Egurrola M, Tamames S, et al. The effectiveness of influenza vaccination in preventing hospitalisations of elderly individuals in two influenza seasons: a multicentre case–control study, Spain, 2013/14 and 2014/15. Euro Surveill. 2017;22(34). doi:10.2807/1560-7917.ES.2017.22.34.30602.
  • Darvishian M, van den Heuvel ER, Bissielo A, Castilla J, Cohen C, Englund H, Gefenaite G, Huang W-T, la Bastide-van Gemert S, Martinez-Baz I, et al. Effectiveness of seasonal influenza vaccination in community-dwelling elderly people: an individual participant data meta-analysis of test-negative design case-control studies. Lancet Respir Med. 2017;5(3):200–11
  • Andrew MK, Shinde V, Ye L, Hatchette T, Haguinet F, Dos Santos G, McElhaney JE, Ambrose A, Boivin G, Bowie W, et al. The Importance of frailty in the assessment of influenza vaccine effectiveness against influenza-related hospitalization in elderly people. J Infect Dis. 2017;216(4):405–14. doi:10.1093/infdis/jix282.
  • Cowling BJ, Feng S, Finelli L, Steffens A, Fowlkes A. Assessment of influenza vaccine effectiveness in a sentinel surveillance network 2010-13, United States. Vaccine. 2016;34(1):61–66. doi:10.1016/j.vaccine.2015.11.016.
  • Moa AM, Chughtai AA, Muscatello DJ, Turner RM, MacIntyre CR. Immunogenicity and safety of inactivated quadrivalent influenza vaccine in adults: A systematic review and meta-analysis of randomised controlled trials. Vaccine. 2016;34(35):4092–102. doi:10.1016/j.vaccine.2016.06.064.
  • Government of Canada. Canadian immunization guide chapter on influenza and statement on seasonal influenza vaccine for 2018–2019. An Advisory Committee Statement (ACS). national advisory committee on immunization (NACI). [ accessed 2019 Jan 16]. https://www.canada.ca/en/public-health/services/publications/healthy-living/canadian-immunization-guide-statement-seasonal-influenza-vaccine-2018-2019.html#5.22018
  • Grohskopf LA, Sokolow LZ, Broder KR, Walter EB, Fry AM, Jernigan DB. Prevention and Control of Seasonal Influenza with vaccines: recommendations of the advisory committee on immunization practices—United States, 2018–19 Influenza Season. MMWR Recomm Rep. 2018;67(RR–3):1–20. doi:10.15585/mmwr.rr6703a1.
  • Australian Government, Department of Health Influenza: the Australian immunizations handbook. Adults aged ≥65 years are strongly recommended to receive either high-dose or adjuvanted influenza vaccine every year. [ accessed 2019 Jan 3]. https://immunisationhandbook.health.gov.au/recommendations/adults-aged-65-years-are-strongly-recommended-to-receive-either-high-dose-or
  • European Centre for Disease Prevention and Control. Types of seasons influenza vaccine. [ accessed 2019 Jan 3]. https://ecdc.europa.eu/en/seasonal-influenza/prevention-and-control/vaccines/types-of-seasonal-influenza-vaccine
  • Izurieta HS, Chillarige Y, Kelman J, Wei Y, Lu Y, Xu W, Lu M, Pratt D, Chu S, Wernecke M, et al. Relative effectiveness of cell-cultured and egg-based influenza vaccines among elderly persons in the United States, 2017-2018. J Infect Dis. 2019;220(8):1255–64. doi:10.1093/infdis/jiy716.
  • Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4(1):1. doi:10.1186/2046-4053-4-1.
  • Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, Savovic J, Schulz KF, Weeks L, Sterne JAC, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomized trials[J]. BMJ. 2011;343:d5928. doi:10.1136/bmj.d5928.
  • Andrade C. Understanding relative risk, odds ratio, and related terms: as simple as it can get. J Clin Psychiatry. 2015;76(7):e857–e861. doi:10.4088/JCP.15f10150.
  • DerSimonian R, Laird N. Meta-analysis in clinical trials revisited. Contemp Clin Trials. 2015;45(Pt A):139–45. doi:10.1016/j.cct.2015.09.002.
  • Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58. doi:10.1002/sim.1186.
  • Wang S-Y, Liu S-Z, Chu K, Zhao Y, Zhu F-C, Hu Y-M, Meng F-Y, Li J-X, Luo L, Yang J-Y, et al. Immunogenicity and safety of an inactivated quadrivalent influenza vaccine candidate versus inactivated trivalent influenza vaccines in participants >/=3 years of age: a double-blind, randomized, parallel-controlled phase III clinical trial in China. Expert Rev Vaccines. 2017;16(11):1155–69. doi:10.1080/14760584.2017.1374181.
  • Melsen WG, Bootsma MC, Rovers MM, Bonten MJM. The effects of clinical and statistical heterogeneity on the predictive values of results from meta-analyses. Clin Microbiol Infect. 2014;20(2):123–29. doi:10.1111/1469-0691.12494.
  • Review Manager (RevMan) [Computer program]. Version 5.3. London (UK): The Nordic Cochrane Centre, The Cochrane Collaboration, 2014.
  • Greenberg DP, Robertson CA, Noss MJ, Blatter MM, Biedenbender R, Decker MD. Safety and immunogenicity of a quadrivalent inactivated influenza vaccine compared to licensed trivalent inactivated influenza vaccines in adults. Vaccine. 2013;31(5):770–76. doi:10.1016/j.vaccine.2012.11.074.
  • Pepin S, Donazzolo Y, Jambrecina A, Salamand C, Saville M. Safety and immunogenicity of a quadrivalent inactivated influenza vaccine in adults. Vaccine. 2013;31(47):5572–78. doi:10.1016/j.vaccine.2013.08.069.
  • Sesay S, Brzostek J, Meyer I, Donazzolo Y, Leroux-Roels G, Rouzier R, Astruc B, Szymanski H, Toursarkissian N, Vandermeulen C, et al. Safety, immunogenicity, and lot-to-lot consistency of a split-virion quadrivalent influenza vaccine in younger and older adults: A phase III randomized, double-blind clinical trial. Hum Vaccin Immunother. 2018;14(3):596–608. doi:10.1080/21645515.2017.1384106.
  • van de Witte S, Nauta J, Montomoli E, Weckx J. A Phase III randomised trial of the immunogenicity and safety of quadrivalent versus trivalent inactivated subunit influenza vaccine in adult and elderly subjects, assessing both anti-haemagglutinin and virus neutralisation antibody responses. Vaccine. 2018;36(40):6030–38. doi:10.1016/j.vaccine.2018.04.043.
  • Sharma S, Singh VB, Kumar S, Prajapati V, Patel J, Vukkala R, Jangid SK, Sanmukhani J, Gupta G, Patel P, et al. Immunogenicity and safety of the first indigenously developed Indian tetravalent influenza vaccine (split virion) in healthy adults ≥ 18 years of age: A randomized, multicenter, phase II / III clinical trial. Hum Vaccin Immunother. 2018;14(6):1362–69. doi:10.1080/21645515.2018.1441654.
  • Tinoco JC, Pavia-Ruz N, Cruz-Valdez A, Aranza Doniz C, Chandrasekaran V, Dewé W, Liu A, Innis BL, Jain VK. Immunogenicity, reactogenicity, and safety of inactivated quadrivalent influenza vaccine candidate versus inactivated trivalent influenza vaccine in healthy adults aged ≥18 years: A phase III, randomized trial. Vaccine. 2014;32(13):1480–87. doi:10.1016/j.vaccine.2014.01.022.
  • Kieninger D, Sheldon E, Lin W-Y, Yu C-J, Bayas JM, Gabor JJ, Esen M, Fernandez Roure JL, Narejos Perez S, Alvarez Sanchez C, et al. Immunogenicity, reactogenicity and safety of an inactivated quadrivalent influenza vaccine candidate versus inactivated trivalent influenza vaccine: a phase III, randomized trial in adults aged ≥18 years. BMC Infect Dis. 2013;13(1):343. doi:10.1186/1471-2334-13-343.
  • Govaert TM, Thijs CT, Masurel N, Sprenger MJ, Dinant GJ, Knottnerus JA. The efficacy of influenza vaccination in elderly individuals: A randomized double-blind placebo-controlled trial. JAMA. 1994;272(21):1661–65. doi:10.1001/jama.1994.03520210045030.
  • Govaert TM, Sprenger MJ, Dinant GJ, Aretz K, Masurel N, Knottnerus JA. Immune response to influenza vaccination of elderly people: A randomized double-blind placebo-controlled trial. Vaccine. 1994;12(13):1185–89. doi:10.1016/0264-410X(94)90241-0.
  • McElhaney JE. Influenza vaccine responses in older adults. Ageing Res Rev. 2011;10(3):379–88. doi:10.1016/j.arr.2010.10.008.
  • McElhaney JE, Ewen C, Zhou X, Kane KP, Xie D, Hager WD, Barry MB, Kleppinger A, Wang Y, Bleackley RC, et al. Granzyme B: correlates with protection and enhanced CTL response to influenza vaccination in older adults. Vaccine. 2009;27(18):2418–25. doi:10.1016/j.vaccine.2009.01.136.
  • Shahid Z, Kleppinger A, Gentleman B, Falsey AR, McElhaney JE. Clinical and immunologic predictors of influenza illness among vaccinated older adults. Vaccine. 2010;28(38):6145–51. doi:10.1016/j.vaccine.2010.07.036.
  • Merani S, Kuchel GA, Kleppinger A, McElhaney JE. Influenza vaccine-mediated protection in older adults: impact of influenza infection, cytomegalovirus serostatus and vaccine dosage. Exp Gerontol. 2018;107:116–25. doi:10.1016/j.exger.2017.09.015.
  • Goodwin K, Viboud C, Simonsen L. Antibody response to influenza vaccination in the elderly: a quantitative review. Vaccine. 2006;24(8):1159–69. doi:10.1016/j.vaccine.2005.08.105.
  • 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. doi:10.1111/j.1750-2659.2011.00268.x.
  • McElhaney JE, Zhou X, Talbot HK, Soethout E, Bleackley RC, Granville DJ, Pawelec G. The unmet need in the elderly: how immunosenescence, CMV infection, co-morbidities and frailty are a challenge for the development of more effective influenza vaccines. Vaccine. 2012;30(12):2060–67. doi:10.1016/j.vaccine.2012.01.015.
  • Leval A, Hergens MP, Persson K, Örtqvist Å. Real-time real-world analysis of seasonal influenza vaccine effectiveness: method development and assessment of a population-based cohort in Stockholm County, Sweden, seasons 2011/12 to 2014/15. Euro Surveill. 2016;21(43). doi:10.2807/1560-7917.ES.2016.21.43.30381.
  • World Health Organization: Seasonal Influenza Fact Sheet 2018. [accessed 2019 Jan 20]. https://www.who.int/en/news-room/fact-sheets/detail/influenza-(seasonal)
  • Centers for Disease Control and Prevention. Early-Season Flu Vaccination Coverage, United States, November 2018. [accessed 2019 Jan 16]. https://www.cdc.gov/flu/fluvaxview/nifs-estimates-nov2018.htm
  • Public Health Agency of Canada. 2016–2017 seasonal influenza vaccine coverage in Canada. [accessed 2019 Jan 16] https://www.canada.ca/en/public-health/services/publications/healthy-living/2016-2017-seasonal-influenza-flu-vaccine-coverage-survey-results.html
  • European Center for Disease Prevention and Control. News & events-> Influenza vaccination coverage rates insufficient across EU Member States. [ accessed 2019 Jan 16]. https://ecdc.europa.eu/en/news-events/influenza-vaccination-coverage-rates-insufficient-across-eu-member-states
  • Karki S, Dyda A, Newall A, Heywood A, MacIntyre CR, McIntyre P, Banks E, Liu B. Comparison of influenza vaccination coverage between immigrant and Australian-born adults. Vaccine. 2016;34(50):6388–95. doi:10.1016/j.vaccine.2016.10.012.
  • Truelove S, Zhu H, Lessler J, Riley S, Read JM, Wang S, Kwok KO, Guan Y, Jiang CQ, Cummings DAT, et al. A comparison of hemagglutination inhibition and neutralization assays for characterizing immunity to seasonal influenza A. Influenza Other Respir Viruses. 2016;10(6):518–24. doi:10.1111/irv.12408.
  • McElhaney JE, Xie D, Hager WD, Barry MB, Wang Y, Kleppinger A, Ewen C, Kane KP, Bleackley RC. T cell responses are better correlates of vaccine protection in the elderly. J Immunol. 2006;176(10):6333–39. doi:10.4049/jimmunol.176.10.6333.