1932

Abstract

Seasonal influenza vaccines prevent influenza-related illnesses, hospitalizations, and deaths. However, these vaccines are not as effective as other viral vaccines, and there is clearly room for improvement. Here, we review the history of seasonal influenza vaccines, describe challenges associated with producing influenza vaccine antigens, and discuss the inherent difficulties of updating influenza vaccine strains each influenza season. We argue that seasonal influenza vaccines can be dramatically improved by modernizing antigen production processes and developing models that are better at predicting viral evolution. Resources should be specifically dedicated to improving seasonal influenza vaccines while developing entirely new vaccine platforms.

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2020-09-29
2024-10-09
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Literature Cited

  1. 1. 
    World Health Organ. 2018. Influenza (seasonal). World Health Organization https://www.who.int/news-room/fact-sheets/detail/influenza-(seasonal)
    [Google Scholar]
  2. 2. 
    Barr IG, Jelley LL. 2012. The coming era of quadrivalent human influenza vaccines. Drugs 72:2177–85
    [Google Scholar]
  3. 3. 
    Cent. Dis. Control 2019. Past seasons vaccine effectiveness estimates. Centers for Disease Control and Prevention https://www.cdc.gov/flu/vaccines-work/past-seasons-estimates.html
    [Google Scholar]
  4. 4. 
    Smith W, Andrewes CH, Laidlaw PP 1933. A virus obtained from influenza patients. Lancet 222:573266–68
    [Google Scholar]
  5. 5. 
    Smorodintseff A, Tushinsky M, Drobyshevskaya A, Korovin A, Osetroff A 1937. Investigation on volunteers infected with the influenza virus. Am. J. Med. Sci. 194:159–70
    [Google Scholar]
  6. 6. 
    Burnet FM. 1937. Influenza virus on the developing egg: IV. The pathogenicity and immunizing power of egg virus for ferrets and mice. Br. J. Exp. Pathol. 18:137–43
    [Google Scholar]
  7. 7. 
    Francis T, Magill TP. 1937. The antibody response of human subjects vaccinated with the virus of human influenza. J. Exp. Med. 65:2251–59
    [Google Scholar]
  8. 8. 
    Stokes J, McGuinness AC, Langner PH, Shaw DR 1937. Vaccination against epidemic influenza with active virus of human influenza. Am. J. Med. Sci. 194:6757–67
    [Google Scholar]
  9. 9. 
    Stokes J, Chenoweth AD, Waltz AD, Gladen RG, Shaw D 1937. Results of immunization by means of active virus of human influenza. J. Clin. Invest. 16:2237–43
    [Google Scholar]
  10. 10. 
    Siegel M, Muckenfuss RS, Schaeffer M, Wilcox HL, Leider AG 1942. A study in active immunization against epidemic influenza and pneumococcus pneumonia at Letchworth Village. IV. Results in an epidemic of influenza A in 1940–41. Am. J. Epidemiol. 35:2186–230
    [Google Scholar]
  11. 11. 
    Francis T. 1953. Vaccination against influenza. Bull. World Health Organ. 8:5–6725–41
    [Google Scholar]
  12. 12. 
    Hirst GK, Rickard ER, Whitman L, Horsfall FL 1942. Antibody response of human beings following vaccination with influenza viruses. J. Exp. Med. 75:5495–511
    [Google Scholar]
  13. 13. 
    Hirst GK. 1941. The agglutination of red cells by allantoic fluid of chick embryos infected with influenza virus. Science 94:242722–23
    [Google Scholar]
  14. 14. 
    Hirst GK. 1942. The quantitative determination of influenza virus and antibodies by means of red cell agglutination. J. Exp. Med. 75:149–64
    [Google Scholar]
  15. 15. 
    Stanley WM. 1944. An evaluation of methods for the concentration and purification of influenza virus. J. Exp. Med. 79:3255–66
    [Google Scholar]
  16. 16. 
    Stanley WM. 1945. The preparation and properties of influenza virus vaccines concentrated and purified by differential centrifugation. J. Exp. Med. 81:2193–218
    [Google Scholar]
  17. 17. 
    Hannoun C. 2013. The evolving history of influenza viruses and influenza vaccines. Expert Rev. Vaccines 12:91085–94
    [Google Scholar]
  18. 18. 
    Glezen WP, Loda FA, Denny FW 1969. A field evaluation of inactivated, zonal-centrifuged influenza vaccines in children in Chapel Hill, North Carolina, 1968–69. Bull. World Health Organ. 41:3566–69
    [Google Scholar]
  19. 19. 
    Barberis I, Myles P, Ault SK, Bragazzi NL, Martini M 2016. History and evolution of influenza control through vaccination: from the first monovalent vaccine to universal vaccines. J. Prev. Med. Hyg. 57:3E115–115
    [Google Scholar]
  20. 20. 
    Groth SFS, Webster RG, Davenport FM 1969. The antigenic subunits of influenza viruses. I. The homologous antibody response. J. Immunol. 103:51099–106
    [Google Scholar]
  21. 21. 
    Brady MI, Furminger IG. 1976. A surface antigen influenza vaccine. 1. Purification of haemagglutinin and neuraminidase proteins. J. Hyg. 77:2161–72
    [Google Scholar]
  22. 22. 
    Wood JM, Schild GC, Newman RW, Seagroatt V 1977. Application of an improved single-radial-immunodiffusion technique for the assay of haemagglutinin antigen content of whole virus and subunit influenza vaccines. Dev. Biol. Stand. 39:193–200
    [Google Scholar]
  23. 23. 
    Schild GC, Wood JM, Newman RW 1975. A single-radial-immunodiffusion technique for the assay of influenza haemagglutinin antigen: proposals for an assay method for the haemagglutinin content of influenza vaccines. Bull. World Health Organ. 52:2223–31
    [Google Scholar]
  24. 24. 
    Ennis FA, Mayner RE, Barry DW, Manischewitz JE, Dunlap RC et al. 1977. Correlation of laboratory studies with clinical responses to A/New Jersey influenza vaccines. J. Infect. Dis. 136:S397–397
    [Google Scholar]
  25. 25. 
    Wright PF, Thompson J, Vaughn WK, Folland DS, Sell SH, Karzon DT 1977. Trials of influenza A/New Jersey/76 virus vaccine in normal children: an overview of age-related antigenicity and reactogenicity. J. Infect. Dis. 136:S731–731
    [Google Scholar]
  26. 26. 
    Henle W, Henle G, Stoker J Jr 1943. Demonstration of the efficacy of vaccination against influenza type A by experimental infection of human beings. J. Immunol. 46:3163–75
    [Google Scholar]
  27. 27. 
    Francis T Jr., Salk JE, Pearson HE, Brown PN 1945. Protective effect of vaccination against induced influenza A. J. Clin. Invest. 24:4536–46
    [Google Scholar]
  28. 28. 
    Salk JE, Pearson HE, Brown PN, Francis T Jr 1945. Protective effect of vaccination against induced influenza B. J. Clin. Invest. 24:4547–53
    [Google Scholar]
  29. 29. 
    Salk JE, Menke WJ Jr., Francis T Jr 1945. A clinical, epidemiological and immunological evaluation of vaccination against epidemic influenza. Am. J. Epidemiol. 42:157–93
    [Google Scholar]
  30. 30. 
    Kilbourne ED. 1969. Future influenza vaccines and the use of genetic recombinants. Bull. World Health Organ. 41:3643–45
    [Google Scholar]
  31. 31. 
    Alexandrova GI, Smorodintsev AA. 1965. Obtaining of an additionally attenuated vaccinating cryophilic influenza strain. Rev. Roum. Inframicrobiol. 2:179–89
    [Google Scholar]
  32. 32. 
    Maassab HF. 1967. Adaptation and growth characteristics of influenza virus at 25° C. Nature 213:5076612–14
    [Google Scholar]
  33. 33. 
    Kendal AP, Maassab HF, Alexandrova GI, Ghendon YZ 1982. Development of cold-adapted recombinant live, attenuated influenza A vaccines in the USA and USSR. Antiviral Res 1:6339–65
    [Google Scholar]
  34. 34. 
    Maassab HF, Kendal AP, Abrams GD, Monto AS 1982. Evaluation of a cold-recombinant influenza virus vaccine in ferrets. J. Infect. Dis. 146:6780–90
    [Google Scholar]
  35. 35. 
    Pebody R, McMenamin J, Nohynek H 2018. Live attenuated influenza vaccine (LAIV): recent effectiveness results from the USA and implications for LAIV programmes elsewhere. Arch. Dis. Child. 103:1101–5
    [Google Scholar]
  36. 36. 
    Skehel JJ, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531–69
    [Google Scholar]
  37. 37. 
    Basak S, Tomana M, Compans RW 1985. Sialic acid is incorporated into influenza hemagglutinin glycoproteins in the absence of viral neuraminidase. Virus Res 2:161–68
    [Google Scholar]
  38. 38. 
    Romero-Beltran L, Baker SF, Puerto-Solís M, González-Losa R, Conde-Ferraez L et al. 2016. Mutations at highly conserved residues in influenza A(H1N1)pdm09 virus affect neuraminidase activity. Virus Res 225:1–9
    [Google Scholar]
  39. 39. 
    Chockalingam AK, Hickman D, Pena L, Ye J, Ferrero A et al. 2012. Deletions in the neuraminidase stalk region of H2N2 and H9N2 avian influenza virus subtypes do not affect postinfluenza secondary bacterial pneumonia. J. Virol. 86:73564–73
    [Google Scholar]
  40. 40. 
    Gao Z, Robinson K, Skowronski DM, De Serres G, Withers SG 2020. Quantification of the total neuraminidase content of recent commercially-available influenza vaccines: introducing a neuraminidase titration reagent. Vaccine 38:4715–18
    [Google Scholar]
  41. 41. 
    Monto AS, Petrie JG, Cross RT, Johnson E, Liu M et al. 2015. Antibody to influenza virus neuraminidase: an independent correlate of protection. J. Infect. Dis. 212:81191–99
    [Google Scholar]
  42. 42. 
    Ng S, Nachbagauer R, Balmaseda A, Stadlbauer D, Ojeda S et al. 2019. Novel correlates of protection against pandemic H1N1 influenza A virus infection. Nat. Med. 25:6962–67
    [Google Scholar]
  43. 43. 
    Hay AJ, Gregory V, Douglas AR, Lin YP 2001. The evolution of human influenza viruses. Philos. Trans. R. Soc. B 356:14161861–70
    [Google Scholar]
  44. 44. 
    Nobusawa E, Sato K. 2006. Comparison of the mutation rates of human influenza A and B viruses. J. Virol. 80:73675–78
    [Google Scholar]
  45. 45. 
    Valesano AL, Fitzsimmons WJ, McCrone JT, Petrie JG, Monto AS et al. 2020. Influenza B viruses exhibit lower within-host diversity than influenza A viruses in human hosts. J. Virol. 94:5e01710-19
    [Google Scholar]
  46. 46. 
    Treanor J. 2004. Influenza vaccine—outmaneuvering antigenic shift and drift. N. Engl. J. Med. 350:3218–20
    [Google Scholar]
  47. 47. 
    Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ et al. 2008. The global circulation of seasonal influenza A (H3N2) viruses. Science 320:5874340–46
    [Google Scholar]
  48. 48. 
    Bedford T, Riley S, Barr IG, Broor S, Chadha M et al. 2015. Global circulation patterns of seasonal influenza viruses vary with antigenic drift. Nature 523:7559217–20
    [Google Scholar]
  49. 49. 
    Ziegler T, Mamahit A, Cox NJ 2018. 65 years of influenza surveillance by a World Health Organization-coordinated global network. Influenza Other Respir. Viruses 12:5558–65
    [Google Scholar]
  50. 50. 
    Barr IG, McCauley J, Cox N, Daniels R, Engelhardt OG et al. 2010. Epidemiological, antigenic and genetic characteristics of seasonal influenza A(H1N1), A(H3N2) and B influenza viruses: basis for the WHO recommendation on the composition of influenza vaccines for use in the 2009–2010 Northern Hemisphere season. Vaccine 28:51156–67
    [Google Scholar]
  51. 51. 
    Jorquera PA, Mishin VP, Chesnokov A, Nguyen HT, Mann B et al. 2019. Insights into the antigenic advancement of influenza A(H3N2) viruses, 2011–2018. Sci. Rep. 9:12676
    [Google Scholar]
  52. 52. 
    Li Y, Myers JL, Bostick DL, Sullivan CB, Madara J et al. 2013. Immune history shapes specificity of pandemic H1N1 influenza antibody responses. J. Exp. Med. 210:81493–500
    [Google Scholar]
  53. 53. 
    Linderman SL, Chambers BS, Zost SJ, Parkhouse K, Li Y et al. 2014. Potential antigenic explanation for atypical H1N1 infections among middle-aged adults during the 2013–2014 influenza season. PNAS 111:4415798–803
    [Google Scholar]
  54. 54. 
    Hensley SE. 2014. Challenges of selecting seasonal influenza vaccine strains for humans with diverse pre-exposure histories. Curr. Opin. Virol. 8:85–89
    [Google Scholar]
  55. 55. 
    Cobey S, Hensley SE. 2017. Immune history and influenza virus susceptibility. Curr. Opin. Virol. 22:105–11
    [Google Scholar]
  56. 56. 
    Petrie JG, Parkhouse K, Ohmit SE, Malosh RE, Monto AS, Hensley SE 2016. Antibodies against the current influenza A(H1N1) vaccine strain do not protect some individuals from infection with contemporary circulating influenza A(H1N1) virus strains. J. Infect. Dis. 214:121947–51
    [Google Scholar]
  57. 57. 
    Gerdil C. 2003. The annual production cycle for influenza vaccine. Vaccine 21:161776–79
    [Google Scholar]
  58. 58. 
    Morris DH, Gostic KM, Pompei S, Bedford T, Łuksza M et al. 2018. Predictive modeling of influenza shows the promise of applied evolutionary biology. Trends Microbiol 26:2102–18
    [Google Scholar]
  59. 59. 
    Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF et al. 2004. Mapping the antigenic and genetic evolution of influenza virus. Science 305:5682371–76
    [Google Scholar]
  60. 60. 
    Łuksza M, Lässig M. 2014. A predictive fitness model for influenza. Nature 507:749057–61
    [Google Scholar]
  61. 61. 
    Steinbruck L, Klingen TR, McHardy AC 2014. Computational prediction of vaccine strains for human influenza A (H3N2) viruses. J. Virol. 88:2012123–32
    [Google Scholar]
  62. 62. 
    Neher RA, Russell CA, Shraiman BI 2014. Predicting evolution from the shape of genealogical trees. eLife 3:e03568
    [Google Scholar]
  63. 63. 
    Bedford T, Huddleston J, Potter B, Neher RA 2019. Seasonal influenza circulation patterns and projections for September 2019 to September 2020. bioRxiv 780627. https://doi.org/10.1101/780627
    [Crossref]
  64. 64. 
    World Health Organ 2018. Recommended composition of influenza virus vaccines for use in the 2019 southern hemisphere influenza season World Health Organ Geneva: https://www.who.int/influenza/vaccines/virus/recommendations/201809_recommendation.pdf
    [Google Scholar]
  65. 65. 
    Wong S-S, Webby RJ. 2013. Traditional and new influenza vaccines. Clin. Microbiol. Rev. 26:3476–92
    [Google Scholar]
  66. 66. 
    Ampofo W, Al Busaidy S, Cox NJ, Giovanni M, Hay A et al. 2013. Strengthening the influenza vaccine virus selection and development process: outcome of the 2nd WHO Informal Consultation for Improving Influenza Vaccine Virus Selection held at the Centre International de Conférences (CICG) Geneva, Switzerland, 7 to 9 December 2011. Vaccine 31:323209–21
    [Google Scholar]
  67. 67. 
    Rogers GN, Paulson JC. 1983. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127:2361–73
    [Google Scholar]
  68. 68. 
    Ito T, Suzuki Y, Takada A, Kawamoto A, Otsuki K et al. 1997. Differences in sialic acid-galactose linkages in the chicken egg amnion and allantois influence human influenza virus receptor specificity and variant selection. J. Virol. 71:43357–62
    [Google Scholar]
  69. 69. 
    Raymond DD, Stewart SM, Lee J, Ferdman J, Bajic G et al. 2016. Influenza immunization elicits antibodies specific for an egg-adapted vaccine strain. Nat. Med. 22:121465–69
    [Google Scholar]
  70. 70. 
    Zost SJ, Parkhouse K, Gumina ME, Kim K, Diaz Perez S et al. 2017. Contemporary H3N2 influenza viruses have a glycosylation site that alters binding of antibodies elicited by egg-adapted vaccine strains. PNAS 114:4712578–83
    [Google Scholar]
  71. 71. 
    Garretson TA, Petrie JG, Martin ET, Monto AS, Hensley SE 2018. Identification of human vaccinees that possess antibodies targeting the egg-adapted hemagglutinin receptor binding site of an H1N1 influenza vaccine strain. Vaccine 36:284095–101
    [Google Scholar]
  72. 72. 
    Wu NC, Zost SJ, Thompson AJ, Oyen D, Nycholat CM et al. 2017. A structural explanation for the low effectiveness of the seasonal influenza H3N2 vaccine. PLOS Pathog 13:10e1006682
    [Google Scholar]
  73. 73. 
    Chambers BS, Parkhouse K, Ross TM, Alby K, Hensley SE 2015. Identification of hemagglutinin residues responsible for H3N2 antigenic drift during the 2014–2015 influenza season. Cell Rep 12:11–6
    [Google Scholar]
  74. 74. 
    Lamb YN. 2019. Cell-based quadrivalent inactivated influenza virus vaccine (Flucelvax® Tetra/Flucelvax Quadrivalent®): a review in the prevention of influenza. Drugs 79:121337–48
    [Google Scholar]
  75. 75. 
    Oh DY, Barr IG, Mosse JA, Laurie KL 2008. MDCK-SIAT1 cells show improved isolation rates for recent human influenza viruses compared to conventional MDCK cells. J. Clin. Microbiol. 46:72189–94
    [Google Scholar]
  76. 76. 
    Lin Y, Wharton SA, Whittaker L, Dai M, Ermetal B et al. 2017. The characteristics and antigenic properties of recently emerged subclade 3C.3a and 3C.2a human influenza A(H3N2) viruses passaged in MDCK cells. Influenza Other Respir. Viruses 11:3263–74
    [Google Scholar]
  77. 77. 
    An Y, Parsons LM, Jankowska E, Melnyk D, Joshi M, Cipollo JF 2019. N-glycosylation of seasonal influenza vaccine hemagglutinins: implication for potency testing and immune processing. J. Virol. 93:2e01693-18
    [Google Scholar]
  78. 78. 
    Cox MMJ, Hollister JR. 2009. FluBlok, a next generation influenza vaccine manufactured in insect cells. Biologicals 37:3182–89
    [Google Scholar]
  79. 79. 
    Gouma S, Zost SJ, Parkhouse K, Branche A, Topham DJ et al. 2019. Comparison of human H3N2 antibody responses elicited by egg-based, cell-based, and recombinant protein-based influenza vaccines during the 2017–2018 season. Clin. Infect. Dis. 2019 ciz996
    [Google Scholar]
  80. 80. 
    Cowling BJ, Perera RAPM, Valkenburg SA, Leung NHL, Iuliano AD et al. 2019. Comparative immunogenicity of several enhanced influenza vaccine options for older adults: a randomized, controlled trial. Clin. Infect. Dis. 2019 ciz1034
    [Google Scholar]
  81. 81. 
    Lu Y, Chillarige Y, Izurieta HS, Wei Y, Xu W et al. 2019. Effect of age on relative effectiveness of high-dose versus standard-dose influenza vaccines among US Medicare beneficiaries aged ≥65 years. J. Infect. Dis. 220:91511–20
    [Google Scholar]
  82. 82. 
    DiazGranados CA, Dunning AJ, Kimmel M, Kirby D, Treanor J et al. 2014. Efficacy of high-dose versus standard-dose influenza vaccine in older adults. N. Engl. J. Med. 371:7635–45
    [Google Scholar]
  83. 83. 
    Cate TR, Rayford Y, Niño D, Niño N, Winokur P et al. 2010. A high dosage influenza vaccine induced significantly more neuraminidase antibody than standard vaccine among elderly subjects. Vaccine 28:2076–79
    [Google Scholar]
  84. 84. 
    Izurieta HS, Thadani N, Shay DK, Lu Y, Maurer A et al. 2015. Comparative effectiveness of high-dose versus standard-dose influenza vaccines in US residents aged 65 years and older from 2012 to 2013 using Medicare data: a retrospective cohort analysis. Lancet Infect. Dis. 15:3293–300
    [Google Scholar]
  85. 85. 
    Shay DK, Chillarige Y, Kelman J, Forshee RA, Foppa IM et al. 2017. Comparative effectiveness of high-dose versus standard-dose influenza vaccines among US Medicare beneficiaries in preventing postinfluenza deaths during 2012–2013 and 2013–2014. J. Infect. Dis. 215:4510–17
    [Google Scholar]
  86. 86. 
    Izurieta HS, Chillarige Y, Kelman J, Wei Y, Lu Y et al. 2018. Relative effectiveness of cell-cultured and egg-based influenza vaccines among elderly persons in the United States, 2017–2018. J. Infect. Dis. 220:81255–64
    [Google Scholar]
  87. 87. 
    Dunkle LM, Izikson R, Patriarca P, Goldenthal KL, Muse D et al. 2017. Efficacy of recombinant influenza vaccine in adults 50 years of age or older. N. Engl. J. Med. 376:252427–36
    [Google Scholar]
  88. 88. 
    Khurana S, Hahn M, Coyle EM, King LR, Lin T-L et al. 2019. Repeat vaccination reduces antibody affinity maturation across different influenza vaccine platforms in humans. Nat. Commun. 10:13338
    [Google Scholar]
  89. 89. 
    Levine MZ, Martin ET, Petrie JG, Lauring AS, Holiday C et al. 2019. Antibodies against egg- and cell-grown influenza A(H3N2) viruses in adults hospitalized during the 2017–2018 influenza season. J. Infect. Dis. 219:121904–12
    [Google Scholar]
  90. 90. 
    Bodewes R, de Mutsert G, van der Klis FRM, Ventresca M, Wilks S et al. 2011. Prevalence of antibodies against seasonal influenza A and B viruses in children in Netherlands. Clin. Vaccine Immunol. 18:3469–76
    [Google Scholar]
  91. 91. 
    Francis T. 1960. On the doctrine of original antigenic sin. Proc. Am. Philos. Soc. 104:6572–78
    [Google Scholar]
  92. 92. 
    Gostic KM, Ambrose M, Worobey M, Lloyd-Smith JO 2016. Potent protection against H5N1 and H7N9 influenza via childhood hemagglutinin imprinting. Science 354:6313722–26
    [Google Scholar]
  93. 93. 
    Skowronski DM, Chambers C, Sabaiduc S, De Serres G, Winter A-L et al. 2017. Beyond antigenic match: possible agent-host and immuno-epidemiological influences on influenza vaccine effectiveness during the 2015–2016 season in Canada. J. Infect. Dis. 216:121487–500
    [Google Scholar]
  94. 94. 
    Jackson ML, Chung JR, Jackson LA, Phillips CH, Benoit J et al. 2017. Influenza vaccine effectiveness in the United States during the 2015–2016 season. N. Engl. J. Med. 377:6534–43
    [Google Scholar]
  95. 95. 
    Arevalo P, Mclean HQ, Belongia EA, Cobey S 2020. Earliest infections predict the age distribution of seasonal influenza A cases. medRxiv 19001875
  96. 96. 
    Skowronski DM, Sabaiduc S, Leir S, Rose C, Zou M et al. 2019. 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 24:461900585
    [Google Scholar]
  97. 97. 
    Kissling E, Pozo F, Buda S, Vilcu A-M, Gherasim A et al. 2019. Low 2018/19 vaccine effectiveness against influenza A(H3N2) among 15–64-year-olds in Europe: exploration by birth cohort. Euro Surveill 24:481900604
    [Google Scholar]
  98. 98. 
    Ohmit SE, Thompson MG, Petrie JG, Thaker SN, Jackson ML et al. 2014. Influenza vaccine effectiveness in the 2011–2012 season: protection against each circulating virus and the effect of prior vaccination on estimates. Clin. Infect. Dis. 58:3319–27
    [Google Scholar]
  99. 99. 
    Skowronski DM, Chambers C, De Serres G, Sabaiduc S, Winter A-L et al. 2017. Serial vaccination and the antigenic distance hypothesis: effects on influenza vaccine effectiveness during A(H3N2) epidemics in Canada, 2010–2011 to 2014–2015. J. Infect. Dis. 215:71059–99
    [Google Scholar]
  100. 100. 
    Ng S, Ip DKM, Fang VJ, Chan K-H, Chiu SS et al. 2013. The effect of age and recent influenza vaccination history on the immunogenicity and efficacy of 2009–10 seasonal trivalent inactivated influenza vaccination in children. PLOS ONE 8:3e59077
    [Google Scholar]
  101. 101. 
    Belongia EA, Skowronski DM, McLean HQ, Chambers C, Sundaram ME, De Serres G 2017. Repeated annual influenza vaccination and vaccine effectiveness: review of evidence. Expert Rev. Vaccines 16:7723–36
    [Google Scholar]
  102. 102. 
    Thompson MG, Naleway A, Fry AM, Ball S, Spencer SM et al. 2016. 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 34:7981–88
    [Google Scholar]
  103. 103. 
    Leung VKY, Carolan LA, Worth LJ, Harper SA, Peck H et al. 2017. Influenza vaccination responses: evaluating impact of repeat vaccination among health care workers. Vaccine 35:192558–68
    [Google Scholar]
  104. 104. 
    Sanyal M, Holmes TH, Maecker HT, Albrecht RA, Dekker CL et al. 2019. Diminished B-cell response after repeat influenza vaccination. J. Infect. Dis. 219:101586–95
    [Google Scholar]
  105. 105. 
    Künzel W, Glathe H, Engelmann H, Van Hoecke C 1996. Kinetics of humoral antibody response to trivalent inactivated split influenza vaccine in subjects previously vaccinated or vaccinated for the first time. Vaccine 14:121108–10
    [Google Scholar]
  106. 106. 
    Nabeshima S, Kashiwagi K, Murata M, Kanamoto Y, Furusyo N, Hayashi J 2007. Antibody response to influenza vaccine in adults vaccinated with identical vaccine strains in consecutive years. J. Med. Virol. 79:3320–25
    [Google Scholar]
  107. 107. 
    Zelner J, Petrie JG, Trangucci R, Martin ET, Monto AS 2019. Effects of sequential influenza A(H1N1)pdm09 vaccination on antibody waning. J. Infect. Dis. 220:112–19
    [Google Scholar]
  108. 108. 
    Andrews SF, Kaur K, Pauli NT, Huang M, Huang Y, Wilson PC 2015. High preexisting serological antibody levels correlate with diversification of the influenza vaccine response. J. Virol. 89:63308–17
    [Google Scholar]
  109. 109. 
    Plant EP, Fredell LJ, Hatcher BA, Li X, Chiang M-J et al. 2017. Different repeat annual influenza vaccinations improve the antibody response to drifted influenza strains. Sci. Rep. 7:15258
    [Google Scholar]
  110. 110. 
    Krammer F, Palese P. 2013. Influenza virus hemagglutinin stalk-based antibodies and vaccines. Curr. Opin. Virol. 3:5521–30
    [Google Scholar]
  111. 111. 
    Worobey M, Plotkin S, Hensley SE 2020. Influenza vaccines delivered in early childhood could turn antigenic sin into antigenic blessings. Cold Spring Harb. Perspect. Med. 21:a03847
    [Google Scholar]
  112. 112. 
    Park JK, Han A, Czajkowski L, Reed S, Athota R et al. 2018. Evaluation of preexisting anti-hemagglutinin stalk antibody as a correlate of protection in a healthy volunteer challenge with influenza A/H1N1pdm virus. mBio 9:1e02284-17
    [Google Scholar]
  113. 113. 
    Christensen SR, Toulmin SA, Griesman T, Lamerato LE, Petrie JG et al. 2019. Assessing the protective potential of H1N1 influenza virus hemagglutinin head and stalk antibodies in humans. J. Virol. 93:8e02134-18
    [Google Scholar]
  114. 114. 
    Bernstein DI, Guptill J, Naficy A, Nachbagauer R, Berlanda-Scorza F et al. 2020. Immunogenicity of chimeric haemagglutinin-based, universal influenza virus vaccine candidates: interim results of a randomised, placebo-controlled, phase 1 clinical trial. Lancet Infect. Dis. 20:180–91
    [Google Scholar]
  115. 115. 
    Couch RB, Atmar RL, Franco LM, Quarles JM, Wells J et al. 2013. Antibody correlates and predictors of immunity to naturally occurring influenza in humans and the importance of antibody to the neuraminidase. J. Infect. Dis. 207:6974–81
    [Google Scholar]
  116. 116. 
    Murphy BR, Kasel JA, Chanock RM 1972. Association of serum anti-neuraminidase antibody with resistance to influenza in man. N. Engl. J. Med. 286:251329–32
    [Google Scholar]
  117. 117. 
    Monto AS, Kendal AP. 1973. Effect of neuraminidase antibody on Hong Kong influenza. Lancet 301:7804623–25
    [Google Scholar]
  118. 118. 
    Memoli MJ, Shaw PA, Han A, Czajkowski L, Reed S et al. 2016. Evaluation of antihemagglutinin and antineuraminidase antibodies as correlates of protection in an influenza A/H1N1 virus healthy human challenge model. mBio 7:2e00417-16
    [Google Scholar]
  119. 119. 
    Krammer F, Fouchier RAM, Eichelberger MC, Webby RJ, Shaw-Saliba K et al. 2018. NAction! How can neuraminidase-based immunity contribute to better influenza virus vaccines. ? mBio 9:2e02332-17
    [Google Scholar]
  120. 120. 
    Kilbourne ED, Johansson BE, Grajower B 1990. Independent and disparate evolution in nature of influenza A virus hemagglutinin and neuraminidase glycoproteins. PNAS 87:2786–90
    [Google Scholar]
  121. 121. 
    Sandbulte MR, Westgeest KB, Gao J, Xu X, Klimov AI et al. 2011. Discordant antigenic drift of neuraminidase and hemagglutinin in H1N1 and H3N2 influenza viruses. PNAS 108:5120748–53
    [Google Scholar]
  122. 122. 
    Chen Y-Q, Wohlbold TJ, Zheng N-Y, Huang M, Huang Y et al. 2018. Influenza infection in humans induces broadly cross-reactive and protective neuraminidase-reactive antibodies. Cell 173:2417–29
    [Google Scholar]
  123. 123. 
    Wan H, Gao J, Yang H, Yang S, Harvey R et al. 2019. The neuraminidase of A(H3N2) influenza viruses circulating since 2016 is antigenically distinct from the A/Hong Kong/4801/2014 vaccine strain. Nat. Microbiol. 4:122216–25
    [Google Scholar]
  124. 124. 
    Dou D, Revol R, Östbye H, Wang H, Daniels R 2018. Influenza A virus cell entry, replication, virion assembly and movement. Front. Immunol. 9:1581
    [Google Scholar]
  125. 125. 
    Treanor JJ, Tierney EL, Zebedee SL, Lamb RA, Murphy BR 1990. Passively transferred monoclonal antibody to the M2 protein inhibits influenza A virus replication in mice. J. Virol. 64:31375–77
    [Google Scholar]
  126. 126. 
    Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W 1999. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat. Med. 5:101157–63
    [Google Scholar]
  127. 127. 
    Padilla-Quirarte HO, Lopez-Guerrero DV, Gutierrez-Xicotencatl L, Esquivel-Guadarrama F 2019. Protective antibodies against influenza proteins. Front. Immunol. 10:1677
    [Google Scholar]
  128. 128. 
    Yewdell JW, Bennink JR, Smith GL, Moss B 1985. Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. PNAS 82:61785–89
    [Google Scholar]
  129. 129. 
    Turley CB, Rupp RE, Johnson C, Taylor DN, Wolfson J et al. 2011. Safety and immunogenicity of a recombinant M2e-flagellin influenza vaccine (STF2.4xM2e) in healthy adults. Vaccine 29:325145–52
    [Google Scholar]
  130. 130. 
    Erbelding EJ, Post DJ, Stemmy EJ, Roberts PC, Augustine AD et al. 2018. A universal influenza vaccine: the strategic plan for the National Institute of Allergy and Infectious Diseases. J. Infect. Dis. 218:3347–54
    [Google Scholar]
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