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Mini-Review

The effect of sex on responses to influenza vaccines

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Pages 1396-1402 | Received 23 Jul 2020, Accepted 23 Sep 2020, Published online: 12 Nov 2020

References

  • Iuliano AD, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, Choen C, Gran JM, Schanzer D, Cowling BJ, Wu P, Kyncl J, Ang LW, Park M, Redlberger-Fritz M, Yu H, Espenhain L, Krishnan A, Emukule G, van Asten L, Pereira da Silva S, Aungkulanon S, Buchholz U, Widdowsen MA, Bresee JS. 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.
  • CDC Seasonal Flu Vaccine Effectiveness Studies. CDC. Available at: https://www.cdc.gov/flu/vaccines-work/effectiveness-studies.htm. (Accessed 16 March 2020)
  • MMR Vaccination. What You Should Know | measles, Mumps, Rubella. CDC. Available at: https://www.cdc.gov/vaccines/vpd/mmr/public/index.html. (Accessed 16 March 2020)
  • Paules CI, Fauci AS. Influenza vaccines: good, but we can do better. J. Infect. Dis. 2019;219(Supplement_1):S1–S4. doi:10.1093/infdis/jiy633.
  • Edwards A. Annual National Flu programme letter 2019 to 2020. 2019.
  • Baxter D. Evaluating the case for trivalent or quadrivalent influenza vaccines. Hum Vaccin Immunother. 2016;12(10):2712–17. doi:10.1080/21645515.2015.1091130.
  • Public Health England (PHE). Guidance. Summary of data to support the choice of influenza vaccination for adults in primary care. 2018.
  • Van Buynder PG, Konrad S, Van Buynder JL, Brodkin E, Krajden M, Ramler G, Bigham M. The comparative effectiveness of adjuvanted and unadjuvanted trivalent inactivated influenza vaccine (TIV) in the elderly. Vaccine. 2013;31(51):6122–28. doi:10.1016/j.vaccine.2013.07.059.
  • Flanagan KL, Fink AL, Plebanski M, Klein SL. Sex and gender differences in the outcomes of vaccination over the life course. Annu. Rev. Cell Dev. Biol. 2017;33(1):577–99. doi:10.1146/annurev-cellbio-100616-060718.
  • Klein SL, Jedlicka A, Pekosz A. The Xs and Y of immune responses to viral vaccines. Lancet Infect Dis. 2010;10(5):338–49. doi:10.1016/S1473-3099(10)70049-9.
  • Markle JG, Fish EN. SeXX matters in immunity. Trends Immunol. 2014;35(3):97–104. doi:10.1016/j.it.2013.10.006.
  • Klein SL, Pekosz A. Sex-based biology and the rational design of influenza vaccination strategies. J. Infect. Dis. 2014;209(suppl 3):S114–S119. doi:10.1093/infdis/jiu066.
  • Klein SL, Marriott I, Fish EN. Sex-based differences in immune function and responses to vaccination. Trans. R. Soc. Trop. Med. Hyg. 2014;109:9–15.
  • Van Der Laan JW, Herberts C, Lambkin-Williams R, Boyers A, Mann AJ, Oxford J. Animal models in influenza vaccine testing. Expert Rev Vaccines. 2008;7(6):783–93. doi:10.1586/14760584.7.6.783.
  • Huber VC, McKeon RM, Brackin MN, Miller LA, Keating R, Brown SA, Makarova N, Perez DR, MacDonald GH, McCullers JA, et al. Distinct contributions of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clin. Vaccine Immunol. 2006;13(9):981–90. doi:10.1128/CVI.00156-06.
  • Plotkin SA. Immunologic correlates of protection induced by vaccination. Pediatric Infect Dis J. 2001;20(1):63–75. doi:10.1097/00006454-200101000-00013.
  • Živković I, Bufan B, Petrušić V, Minić R, Arsenović-Ranin N, Petrović R, Leposavić G. Sexual diergism in antibody response to whole virus trivalent inactivated influenza vaccine in outbred mice. Vaccine. 2015;33(42):5546–52. doi:10.1016/j.vaccine.2015.09.006.
  • Živković I, Petrović R, Arsenović-Ranin N, Petrušić V, Minić R, Bufan B, Popović O, Leposavić G. Sex bias in mouse humoral immune response to influenza vaccine depends on the vaccine type. Biologicals. 2018;52:18–24. doi:10.1016/j.biologicals.2018.01.007.
  • Petrović R, Bufan B, Arsenović-Ranin N, Živković I, Minić R, Radojević K, Leposavić G. Mouse strain and sex as determinants of immune response to trivalent influenza vaccine. Life Sci. 2018;207:117–26. doi:10.1016/j.lfs.2018.05.056.
  • Arsenović-Ranin N, Petrović R, Živković I, Bufan B, Stoiljković V, Leposavić G. Influence of aging on germinal centre reaction and antibody response to inactivated influenza virus antigens in mice: sex-based differences. Biogerontology. 2019;20(4):475–96. doi:10.1007/s10522-019-09811-8.
  • Fink AL, Engle K, Ursin RL, Tang WY, Klein SL. Biological sex affects vaccine efficacy and protection against influenza in mice. Proc. Natl. Acad. Sci. U. S. A. 2018;115(49):12477–82. doi:10.1073/pnas.1805268115.
  • Potluri T, Fink AL, Sylvia KE, Dhakal S, Vermillion MS, vom Steeg L, Deshpande S, Narasimhan H, Klein SL. Age-associated changes in the impact of sex steroids on influenza vaccine responses in males and females. Npj Vaccines. 2019;4.
  • Lorenzo ME, Hodgson A, Robinson DP, Kaplan JB, Pekosz A, Klein SL. Antibody responses and cross protection against lethal influenza A viruses differ between the sexes in C57BL/6 mice. Vaccine. 2011;29(49):9246–55. doi:10.1016/j.vaccine.2011.09.110.
  • Luke CJ, Subbarao K. The role of animal models in influenza vaccine research. Influenza vaccines for the future, 161–202. Birkhäuser Basel. 2008. 10.1007/978-3-7643-8371-8_8
  • Furman D, Hejblum BP, Simon N, Jojic V, Dekker CL, Thiebaut R, Tibshirani RJ, Davis MM. Systems analysis of sex differences reveals an immunosuppressive role for testosterone in the response to influenza vaccination. Proc. Natl. Acad. Sci. U. S. A. 2014;111(2):869–74. doi:10.1073/pnas.1321060111.
  • Cook IF, Barr I, Hartel G, Pond D, Hampson AW. Reactogenicity and immunogenicity of an inactivated influenza vaccine administered by intramuscular or subcutaneous injection in elderly adults. Vaccine. 2006;24(13):2395–402. doi:10.1016/j.vaccine.2005.11.057.
  • Falsey AR, Treanor JJ, Tornieporth N, Capellan J, Gorse GJ. Randomized, double‐blind controlled phase 3 trial comparing the immunogenicity of high‐dose and standard‐dose influenza vaccine in adults 65 years of age and older. J. Infect. Dis. 2009;200(2):172–80. doi:10.1086/599790.
  • Hara M, Hanaoka T, Maeda K, Kase T, Ohfuji S, Fukushima W, Hirota Y. Immunogenicity and efficacy of A/H1N1pdm vaccine among subjects with severe motor and intellectual disability in the 2010/11 influenza season. J. Epidemiol. 2016;26(6):300–06. doi:10.2188/jea.JE20150036.
  • Talaat KR, Greenberg M, Lai M, Hartel G, Wichems C, Rockman S, Jeanfreau R, Ghosh M, Kabongo M, Gittleson C, et al. A single dose of unadjuvanted novel 2009 H1N1 vaccine is immunogenic and well tolerated in young and elderly adults. J. Infect. Dis. 2010;202(9):1327–37. doi:10.1086/656601.
  • Fink AL, Klein SL. Sex and gender impact immune responses to vaccines among the elderly. Physiology. 2015;30(6):408–16. doi:10.1152/physiol.00035.2015.
  • Looker C, Luster MI, Calafat AM, Johnson VJ, Burleson GR, Burleson FG, Fletcher T. Influenza vaccine response in adults exposed to perfluorooctanoate and perfluorooctanesulfonate. Toxicol. Sci. 2014;138(1):76–88. doi:10.1093/toxsci/kft269.
  • Jackson LA, Gaglani MJ, Keyserling HL, Balser J, Bouveret N, Fries L, Treanor JJ. Safety, efficacy, and immunogenicity of an inactivated influenza vaccine in healthy adults: A randomized, placebo-controlled trial over two influenza seasons. BMC Infect. Dis. 2010;10(1). doi:10.1186/1471-2334-10-71.
  • Olafsdottir TA, Alexandersson KF, Sveinbjornsson G, Lapini G, Palladino L, Montomoli E, Del Giudice G, Gudbjartsson DF, Jonsdottir I. Age and influenza-specific pre-vaccination antibodies strongly affect influenza vaccine responses in the icelandic population whereas disease and medication have small effects. Front. Immunol. 2018;8:1872. doi:10.3389/fimmu.2017.01872.
  • Hagihara Y, Ohfuji S, Watanabe K, Yamagami H, Fukushima, W, Maeda K, Kamata N, Sogawa M, Shiba M, Tanigawa T, Tominaga K, Watanabe T, Fujiwara Y, Hirota Y, Arakawa T. Infliximab and/or immunomodulators inhibit immune responses to trivalent influenza vaccination in adults with inflammatory bowel disease. J. Crohn’s Colitis. 2014;8(3):223–33. doi:10.1016/j.crohns.2013.08.008.
  • Rapezzi D, Sticchi L, Racchi O, Mangerini R, Ferraris AM, Gaetani GF. Influenza vaccine in chronic lymphoproliferative disorders and multiple myeloma. Eur. J. Haematol. 2003;70(4):225–30. doi:10.1034/j.1600-0609.2003.00028.x.
  • Gorse GJ, Falsey AR, Ozol-Godfrey A, Landolfi V, Tsang PH. Safety and immunogenicity of a quadrivalent intradermal influenza vaccine in adults. Vaccine. 2015;33(9):1151–59. doi:10.1016/j.vaccine.2015.01.025.
  • Coleman BL, McGeer AJ, Halperin SA, Langley JM, Shamout Y, Taddio A, Shah V, McNeil SA. A randomized control trial comparing immunogenicity, safety, and preference for self- versus nurse-administered intradermal influenza vaccine. Vaccine. 2012;30(44):6287–93. doi:10.1016/j.vaccine.2012.08.006.
  • Nakaya HI, Hagan T, Duraisingham S, Lee E, Kwissa M, Rouphael N, Frasca D, Gersten M, Mehta A, Gaujoux R, et al. Systems analysis of immunity to influenza vaccination across multiple years and in diverse populations reveals shared molecular signatures. Immunity. 2015;43(6):1186–98. doi:10.1016/j.immuni.2015.11.012.
  • Moynihan JA, Larson MR, Treanor J, Duberstein PR, Power A, Shore B, Ader R. Psychosocial factors and the response to influenza vaccination in older adults. Psychosom. Med. 2004;66(6):950–53. doi:10.1097/01.psy.0000140001.49208.2d.
  • Strindhall J, Ernerudh J, Mörner A, Waalen K, Löfgren S, Matussek A, Bengner M. Humoral response to influenza vaccination in relation to pre-vaccination antibody titres, vaccination history, cytomegalovirus serostatus and CD4/CD8 ratio. Infect. Dis. (Auckl). 2016;48(6):436–42. doi:10.3109/23744235.2015.1135252.
  • Govaert TME, Sprenger MJW, 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.
  • Barrett PN, Berezuk G, Fritsch S, Aichinger G, Hart MK, El-Amin W, Kistner O, Ehrlich HJ. Efficacy, safety, and immunogenicity of a Vero-cell-culture-derived trivalent influenza vaccine: A multicentre, double-blind, randomised, placebo-controlled trial. Lancet. 2011;377(9767):751–59. doi:10.1016/S0140-6736(10)62228-3.
  • Rivera L, Mazara S, Vargas M, Fragapane E, Casula D, Groth N. Phase III, randomized controlled trial to evaluate lot consistency of a trivalent subunit egg-based influenza vaccine in adults. Vaccine. 2012;30(35):5285–92. doi:10.1016/j.vaccine.2012.05.021.
  • Tadount F, Doyon-Plourde P, Rafferty E, MacDonald S, Sadarangani M, Quach C. Is there a difference in the immune response, efficacy, effectiveness and safety of seasonal influenza vaccine in males and females? – A systematic review. Vaccine. 2019. doi:10.1016/j.vaccine.2019.10.091.
  • Ferdinands JM, Shay DK. Magnitude of potential biases in a simulated case-control study of the effectiveness of influenza vaccination. Clin. Infect. Dis. 2012;54(1):25–32. doi:10.1093/cid/cir750.
  • Voysey M, Pollard AJ, Perera R, Fanshawe TR. Assessing sex-differences and the effect of timing of vaccination on immunogenicity, reactogenicity and efficacy of vaccines in young children: study protocol for an individual participant data meta-analysis of randomised controlled trials. BMJ Open. 2016;6(7):e011680. doi:10.1136/bmjopen-2016-011680.
  • Mosterín Höpping A, McElhaney J, Fonville JM, Powers DC, Beyer WEP, Smith DJ. The confounded effects of age and exposure history in response to influenza vaccination. Vaccine. 2016;34(4):540–46. doi:10.1016/j.vaccine.2015.11.058.
  • How Flu Vaccine Effectiveness and Efficacy are Measured. CDC. Available at: https://www.cdc.gov/flu/vaccines-work/effectivenessqa.htm. (Accessed 1 January 2020)
  • Mcneil S. Overview of vaccine efficacy and vaccine effectiveness.
  • Mori M, Oura A, Ohnishi H, Washio M. Confounding in evaluating the effectiveness of influenza vaccine. Vaccine. 2008;26(50):6459–61. doi:10.1016/j.vaccine.2008.06.040.
  • Vila-Córcoles A, Rodriguez T, de Diego C, Ochoa O, Valdivieso A, Salsench E, Ansa X, Badía W, Saún N. Effect of influenza vaccine status on winter mortality in Spanish community-dwelling elderly people during 2002-2005 influenza periods. Vaccine. 2007;25(37–38):6699–707. doi:10.1016/j.vaccine.2007.07.015.
  • Fleming DM, Watson JM, Nicholas S, Smith GE, Swan AV. Study of the effectiveness of influenza vaccination in the elderly in the epidemic of 1989–90 using a general practice database. Epidemiol. Infect. 1995;115:581–89.
  • Nichol KL, Nordin JD, Nelson DB, Mullooly JP, Hak E. Effectiveness of influenza vaccine in the community-dwelling elderly. N. Engl. J. Med. 2007;357:1373–81.
  • Nichol KL. Heterogeneity of influenza case definitions and implications for interpreting and comparing study results. Vaccine. 2006;24(44–46):6726–28. doi:10.1016/j.vaccine.2006.05.064.
  • Kwong JC, Campitelli MA, Gubbay JB, Peci A, Winter A-L, Olsha R, Turner R, Rosella LC, Crowcroft NS. Vaccine effectiveness against laboratory-confirmed influenza hospitalizations among elderly adults during the 2010-2011 season. Clin. Infect. Dis. 2013;57(6):820–27. doi:10.1093/cid/cit404.
  • Talbot HK, Griffin MR, Chen Q, Zhu Y, Williams JV, Edwards KM. Effectiveness of seasonal vaccine in preventing confirmed influenza-associated hospitalizations in community dwelling older adults. J. Infect. Dis. 2011;203(4):500–08. doi:10.1093/infdis/jiq076.
  • Trebbien R, Fischer TK, Krause TG, Nielsen L, Nielsen XC, Weinreich LS, Lis-Tønder J, Skov MN, Christiansen CB, Emborg H-D, et al. Changes in genetically drifted H3N2 influenza A viruses and vaccine effectiveness in adults 65 years and older during the 2016/17 season in Denmark. J. Clin. Virol. 2017;94:1–7. doi:10.1016/j.jcv.2017.06.007.
  • Gilca R, Skowronski DM, Douville-Fradet M, Amini R, Boulianne N, Rouleau I, Martineau C, Charest H, De Serres G. Mid-Season estimates of influenza vaccine effectiveness against influenza A(H3N2) hospitalization in the elderly in Quebec, Canada, January 2015. PLoS One. 2015;10(7):e0132195. doi:10.1371/journal.pone.0132195.
  • Bragstad K, Emborg HD, Fischer TK, Voldstedlund M, Gubbels S, Andersen B, Molbak K, Krause TG. Low vaccine effectiveness against influenza A(H3N2) virus among elderly people in Denmark in 2012/13 - A rapid epidemiological and virological assessment. Eurosurveillance. 2013;18:20397.
  • Emborg HD, Krause TG, Nielsen L, Thomsen MK, Christiansen CB, Skov MN, Nielsen XC, Weinreich LS, Fischer TK, Rønn J, et al. Influenza vaccine effectiveness in adults 65 years and older, Denmark, 2015/16 – a rapid epidemiological and virological assessment. Eurosurveillance. 2016;21(14):30189. doi:10.2807/1560-7917.ES.2016.21.14.30189.
  • Galdas PM, Cheater F, Marshall P. Men and health help-seeking behaviour: literature review. J Adv Nurs. 2005;49(6):616–23. doi:10.1111/j.1365-2648.2004.03331.x.
  • Trombetta CM, Gianchecchi E, Montomoli E. Influenza vaccines: evaluation of the safety profile. Hum Vaccin Immunother. 2018;14(3):657–70. doi:10.1080/21645515.2017.1423153.
  • Li R, Stewart B, McNeil MM, Duffy J, Nelson J, Kawai AT, Baxter R, Belongia EA, Weintraub E. Post licensure surveillance of influenza vaccines in the vaccine safety datalink in the 2013–2014 and 2014–2015 seasons. Pharmacoepidemiol. Drug Saf. 2016;25(8):928–34. doi:10.1002/pds.3996.
  • Schmid P, Rauber D, Betsch C, Lidolt G, Denker ML. Barriers of influenza vaccination intention and behavior - A systematic review of influenza vaccine hesitancy, 2005-2016. PLoS ONE. 2017;12.
  • Marti M, de Cola M, MacDonald NE, Dumolard L, Duclos P. Assessments of global drivers of vaccine hesitancy in 2014—Looking beyond safety concerns. PLoS One. 2017;12:e0172310.
  • Engler RJM, Nelson MR, Klote MM, VanRaden MJ, Huang C, Cox NJ, Klimov A, Keitel WA, Nichol KL, Carr WW, Treanor JT. Half- vs full-dose trivalent inactivated influenza vaccine (2004-2005): age, dose, and sex effects on immune responses. Arch. Intern. Med. 2008;168(22):2405–14. doi:10.1001/archinternmed.2008.513.

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