1,395
Views
0
CrossRef citations to date
0
Altmetric
Vaccines

The association between influenza vaccine effectiveness and egg-based manufacturing technology: literature review and US expert consensus

, , , , , , , , ORCID Icon, , , & ORCID Icon show all
Pages 335-343 | Received 25 Jul 2023, Accepted 13 Nov 2023, Published online: 06 Dec 2023

References

  • Centers for Disease Control and Prevention. Past seasons estimated influenza disease burden. 2022. https://www.cdc.gov/flu/about/burden/past-seasons.html
  • Centers for Disease Control and Prevention. Past seasons VE estimates. 2022. https://www.cdc.gov/flu/vaccines-work/effectiveness-studies.htm#figure
  • Belongia EA, Simpson MD, King JP, et al. Variable influenza VE 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.
  • Osterholm MT, Kelley NS, Sommer A, et al. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12(1):36–44. doi:10.1016/S1473-3099(11)70295-X.
  • Okoli GN, Racovitan F, Abdulwahid T, et al. Variable seasonal influenza vaccine effectiveness across geographical regions, age groups and levels of vaccine antigenic similarity with circulating virus strains: a systematic review and meta-analysis of the evidence from test-negative design studies after the 2009/10 influenza pandemic. Vaccine. 2021;39(8):1225–1240. doi:10.1016/j.vaccine.2021.01.032.
  • Skowronski DM, Chambers C, Sabaiduc S, 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. doi:10.1093/cid/ciw176.
  • Tosh PK, Jacobson RM, Poland GA. Influenza vaccines: from surveillance through production to protection. Mayo Clin Proc. 2010;85(3):257–273. doi:10.4065/mcp.2009.0615.
  • Flannery B, Zimmerman RK, Gubareva LV, et al. Enhanced genetic characterization of influenza A(H3N2) viruses and vaccine effectiveness by genetic group, 2014–2015. J Infect Dis. 2016;214(7):1010–1019. doi:10.1093/infdis/jiw181.
  • Raymond DD, Stewart SM, Lee J, et al. Influenza immunization elicits antibodies specific for an egg-adapted vaccine strain. Nat Med. 2016;22(12):1465–1469. doi:10.1038/nm.4223.
  • Centers for Disease Control and Prevention. Vaccine effectiveness: how well do the flu vaccines work? 2021. 2022. https://www.cdc.gov/flu/vaccines-work/vaccineeffect.htm
  • Oxford JS, Newman R, Corcoran T, et al. Direct isolation in eggs of influenza A (H1N1) and B viruses with haemagglutinins of different antigenic and amino acid composition. J Gen Virol. 1991;72(Pt 1):185–189. doi:10.1099/0022-1317-72-1-185.
  • Kishida D, Fujisaki S, Yokoyama M, et al. Evaluation of influenza virus a/H3N2 and B vaccines on the basis of crossreactivity of postvaccination human serum antibodies against influenza viruses a/H3N2 and B isolated in MDCK cells and embryonated hen eggs. Clin Vaccine Immunol. 2012;19(6):897–908. doi:10.1128/CVI.05726-11.
  • Kodihalli S, Justewicz DM, Gubareva LV, et al. Selection of a single amino acid substitution in the hemagglutinin molecule by chicken eggs can render influenza a virus (H3) candidate vaccine ineffective. J Virol. 1995;69(8):4888–4897. doi:10.1128/JVI.69.8.4888-4897.1995.
  • Katz JM, Webster RG. Efficacy of inactivated influenza a virus (H3N2) vaccines grown in mammalian cells or embryonated eggs. J Infect Dis. 1989;160(2):191–198. doi:10.1093/infdis/160.2.191.
  • Robertson JS, Cook P, Nicolson C, et al. Mixed populations in influenza virus vaccine strains. Vaccine. 1994;12(14):1317–1322. doi:10.1016/s0264-410x(94)80058-8.
  • Wood JM, Oxford JS, Dunleavy U, et al. Influenza A (H1N1) vaccine efficacy in animal models is influenced by two amino acid substitutions in the hemagglutinin molecule. Virology. 1989;171(1):214–221. doi:10.1016/0042-6822(89)90528-x.
  • Wu NC, Zost SJ, Thompson AJ, et al. A structural explanation for the low effectiveness of the seasonal influenza H3N2 vaccine. PLoS Pathog. 2017;13(10):e1006682–e1006682. doi:10.1371/journal.ppat.1006682.
  • Barr IG, Russell C, Besselaar TG, et al. WHO recommendations for the viruses used in the 2013–2014 Northern hemisphere influenza vaccine: epidemiology, antigenic and genetic characteristics of influenza A(H1N1)pdm09, A(H3N2) and B influenza viruses collected from october 2012 to january 2013. Vaccine. 2014;32(37):4713–4725. doi:10.1016/j.vaccine.2014.02.014.
  • Centers for Disease Control and Prevention. How influenza (flu) vaccines are made. 2022. https://www.cdc.gov/flu/prevent/how-fluvaccine-made.htm
  • Carrat F, Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine. 2007;25(39-40):6852–6862. doi:10.1016/j.vaccine.2007.07.027.
  • Weir JP, Gruber MF. An overview of the regulation of influenza vaccines in the United States. Influenza Other Respir Viruses. 2016;10(5):354–360. doi:10.1111/irv.12383.
  • Park YW, Kim YH, Jung HU, et al. Comparison of antigenic mutation during egg and cell passage cultivation of H3N2 in-fluenza virus. Clin Exp Vaccine Res. 2020;9(1):56–63. doi:10.7774/cevr.2020.9.1.56.
  • Parker L, Wharton SA, Martin SR, et al. Effects of egg adaptation on receptor-binding and antigenic properties of recent influenza A (H3N2) vaccine viruses. J Gen Virol. 2016;97(6):1333–1344. doi:10.1099/jgv.0.000457.
  • Harding AT, Heaton NS. Efforts to improve the seasonal influenza vaccine. Vaccines. 2018;6(2):19. doi:10.3390/vaccines6020019.
  • Skowronski DM, Janjua NZ, De Serres G, 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. doi:10.1371/journal.pone.0092153.
  • Wang ML, Katz JM, Webster RG. Extensive heterogeneity in the hemagglutinin of egg-grown influenza viruses from different patients. Virology. 1989;171(1):275–279. doi:10.1016/0042-6822(89)90538-2.
  • Boikos C, Fischer L, O'Brien D, et al. Relative effectiveness of the cell-derived inactivated quadrivalent influenza vaccine versus egg-derived inactivated quadrivalent influenza vaccines in preventing influenza-related medical encounters during the 2018–2019 influenza season in the United States. Clin Infect Dis. 2021;73(3):e692–e698. doi:10.1093/cid/ciaa1944.
  • Divino V, Krishnarajah G, Pelton SI, et al. A real-world study evaluating the relative vaccine effectiveness of a cell-based quadrivalent influenza vaccine compared to egg-based quadrivalent influenza vaccine in the US during the 2017–18 influenza season. Vaccine. 2020;38(40):6334–6343. doi:10.1016/j.vaccine.2020.07.023.
  • Paules CI, Sullivan SG, Subbarao K, et al. Chasing seasonal influenza—the need for a universal influenza vaccine. N Engl J Med. 2018;378(1):7–9. doi:10.1056/NEJMp1714916.
  • McLean HQ, Thompson MG, Sundaram ME, et al. Influenza vaccine effectiveness in the United States during 2012–2013: variable protection by age and virus type. J Infect Dis. 2015;211(10):1529–1540. doi:10.1093/infdis/jiu647.
  • Zost SJ, Parkhouse K, Gumina ME, et al. Contemporary H3N2 influenza viruses have a glycosylation site that alters binding of antibodies elicited by egg-adapted vaccine strains. Proc Natl Acad Sci U S A. 2017;114(47):12578–12583. doi:10.1073/pnas.1712377114.
  • 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. doi:10.1093/cid/ciy097.
  • Garten R, Blanton L, Elal AI, et al. Update: influenza activity in the United States during the 2017–18 season and composition of the 2018–19 influenza vaccine. MMWR Morb Mortal Wkly Rep. 2018;67(22):634–642. doi:10.15585/mmwr.mm6722a4externalicon.
  • Petrie JG, Gordon A. Epidemiological studies to support the development of next generation influenza vaccines. Vaccines. 2018;6(2):17. doi:10.3390/vaccines6020017.
  • Ortiz de Lejarazu-Leonardo R, Montomoli E, Wojcik R, et al. Estimation of reduction in influenza vaccine effectiveness due to egg-adaptation changes—systematic literature review and expert consensus. Vaccines. 2021;9(11):1255. doi:10.3390/vaccines9111255.
  • Skowronski DM, Chambers C, Sabaiduc S, et al. Beyond antigenic match: possible agent-host and immuno-epidemiological influences on influenza vaccine effectiveness during the 2015–2016 season in Canada. J Infect Dis. 2017;216(12):1487–1500. doi:10.1093/infdis/jix526.
  • Rajaram S, Wojcik R, Moore C, et al. The impact of candidate influenza virus and egg-based manufacture on vaccine effectiveness: literature review and expert consensus. Vaccine. 2020;38(38):6047–6056. doi:10.1016/j.vaccine.2020.06.021.
  • Jandhyala R. A novel method for observing proportional group awareness and consensus of items arising from list-generating questioning. Curr Med Res Opin. 2020;36(5):883–893. doi:10.1080/03007995.2020.1734920.
  • Jandhyala R. Delphi, non-RAND modified delphi, RAND/UCLA appropriateness method and a novel group awareness and consensus methodology for consensus measurement: a systematic literature review. Curr Med Res Opin. 2020;36(11):1873–1887. doi:10.1080/03007995.2020.1816946.
  • Jandhyala R. Concordance between the schedule for the evaluation of individual quality of life – direct weighting (SEIQoL-DW) and the EuroQoL-5D (EQ-5D) measures of quality of life outcomes in adults with X-linked hypophosphatemia. Orphanet J Rare Dis. 2022;17(1):81. doi:10.1186/s13023-022-02250-8.
  • Damy T, Conceição I, García-Pavía P, et al. A simple core dataset and disease severity score for hereditary transthyretin (ATTRv) amyloidosis. Amyloid. 2021;28(3):189–198. Epub 2021 May 27.PMID: 34042016 doi:10.1080/13506129.2021.1931099.
  • Freedman S, de-Madaria E, Singh VK, et al. A simple core dataset for triglyceride-induced acute pancreatitis. Curr Med Res Opin. 2023;39(1):37–46. doi:10.1080/03007995.2022.2144054.
  • Altman MO, Angeletti D, Yewdell JW. Antibody immunodominance: the key to understanding influenza virus antigenic drift. Viral Immunol. 2018;31(2):142–149. doi:10.1089/vim.2017.0129.
  • Shen J, Ma J, Wang Q. Evolutionary trends of A(H1N1) influenza virus hemagglutinin since 1918. PLoS One. 2009;4(11):e7789. doi:10.1371/journal.pone.0007789.
  • Hardy I, Li Y, Coulthart MB, et al. Molecular evolution of influenza a/H3N2 viruses in the province of québec (Canada) during the 1997–2000 period. Virus Res. 2001;77(1):89–96. doi:10.1016/S0168-1702(01)00269-6.
  • Bragstad K, Nielsen LP, Fomsgaard A. The evolution of human influenza a viruses from 1999 to 2006: a complete genome study. Virol J. 2008;5(1):40. doi:10.1186/1743-422X-5-40.
  • Venter M, Naidoo D, Pretorius M, et al. Evolutionary dynamics of 2009 pandemic influenza a virus subtype H1N1 in South Africa during 2009-2010. J Infect Dis. 2012;20(suppl_1):S166–S172. doi:10.1093/infdis/jis539.
  • Yohannes K, Roche P, Hampson A, et al. Annual report of the national influenza surveillance scheme. Commun Dis Intell Q Rep. 2004;28(2):160–168.
  • Vijaykrishna D, Holmes EC, Joseph U, et al. The contrasting phylodynamics of human influenza B viruses. Elife. 2015;4:e05055. doi:10.7554/eLife.05055.
  • Smith DJ, Lapedes AS, de Jong JC, et al. Mapping the antigenic and genetic evolution of influenza virus. Science. 2004;305(5682):371–376. doi:10.1126/science.1097211.
  • Bedford T, Suchard MA, Lemey P, et al. Integrating influenza antigenic dynamics with molecular evolution. Elife. 2014;3:e01914. doi:10.7554/eLife.01914e01914.
  • Sleigh MJ, Both GW, Underwood PA, et al. Antigenic drift in the hemagglutinin of the Hong Kong influenza subtype: correlation of amino acid changes with alterations in viral antigenicity. J Virol. 1981;37(3):845–853. doi:10.1128/JVI.37.3.845-853.1981.
  • Tenforde MW, Kondor RJG, Chung JR, et al. Effect of antigenic drift on influenza vaccine effectiveness in the United States—2019–2020. Clin Infect Dis. 2021;73(11):e4244–e4250. doi:10.1093/cid/ciaa1884.
  • Ampofo WK, Baylor N, Cobey S, WHO Writing Group., et al. Improving influenza vaccine virus selection: report of a WHO informal consultation held at WHO headquarters, Geneva, Switzerland, 14-16 june 2010. Influenza Resp Viruses. 2012;6(2):142–152, e1-5. doi:10.1111/j.1750-2659.2011.00277.x.
  • Milián E, Kamen AA. Current and emerging cell culture manufacturing technologies for influenza vaccines. Biomed Res Int. 2015;2015:504831–504811. doi:10.1155/2015/504831.
  • Shin D, Park KJ, Lee H, et al. Comparison of immunogenicity of cell-and egg-passaged viruses for manufacturing MDCK cell culture-based influenza vaccines. Virus Res. 2015;204:40–46. doi:10.1016/j.virusres.2015.04.005.
  • Wei CJ, Crank MC, Shiver J, et al. Next-generation influenza vaccines: opportunities and challenges. Nat Rev Drug Discov. 2020;19(4):239–252. doi:10.1038/s41573-019-0056-x.
  • Wahid R, Holt R, Hjorth R, et al. Chemistry, manufacturing and control (CMC) and clinical trial technical support for influenza vaccine manufacturers. Vaccine. 2016;34(45):5430–5435. doi:10.1016/j.vaccine.2016.07.046.
  • Trombetta CM, Marchi S, Manini I, et al. Challenges in the development of egg-independent vaccines for influenza. Expert Rev Vaccines. 2019;18(7):737–750. doi:10.1080/14760584.2019.1639503.
  • Treanor J. Weathering the influenza vaccine crisis. N Engl J Med. 2004;351(20):2037–2040. doi:10.1056/NEJMp048290.
  • Weir JP, Gruber MF. An overview of the regulation of influenza vaccines in the United States. Influenza Other Respir Viruses. 2016;10(5):354–360. doi:10.1111/irv.12383.
  • Gerdil C. The annual production cycle for influenza vaccine. Vaccine. 2003;21(16):1776–1779. doi:10.1016/S0264-410X(03)00071-9.
  • Rocha E, Xu X, Hall H, et al. Comparison of 10 influenza A (H1N1 and H3N2) haemagglutinin sequences obtained directly from clinical specimens to those of MDCK cell- and egg-grown viruses. J Gen Virol. 1993;74 (Pt 11)(11):2513–2518. online doi:10.1099/0022-1317-74-11-2513.
  • Robertson JS, Bootman JS, Newman R, et al. Structural changes in the haemagglutinin which accompany egg adaptation of an influenza A(H1N1) virus. Virology. 1987;160(1):31–37. doi:10.1016/0042-6822(87)90040-7.
  • Stevens J, Chen LM, Carney PJ, et al. Receptor specificity of influenza a H3N2 viruses isolated in mammalian cells and embryonated chicken eggs. J Virol. 2010;84(16):8287–8299. doi:10.1128/JVI.00058-10.
  • Feldman RA, Fuhr R, Smolenov I, et al. mRNA vaccines against H10N8 and H7N9 influenza viruses of pandemic potential are immunogenic and well tolerated in healthy adults in phase 1 randomized clinical trials. Vaccine. 2019;37(25):3326–3334. doi:10.1016/j.vaccine.2019.04.074.
  • ModernaTX I. A Phase 1/2, randomized, stratified, observer-blind, dose-ranging study to evaluate the safety, reactogenicity, and immunogenicity of mRNA-1010 seasonal influenza vaccine in healthy adults 18 years and older. 2021. https://clinicaltrials.gov/ct2/show/NCT04956575.
  • Dolgin E. mRNA flu shots move into trials. Nat Rev Drug Discov. 2021;20(11):801–803. doi:10.1038/d41573-021-00176-7.
  • Jeeva S, Kim KH, Shin CH, et al. An update on mRNA-based viral vaccines. Vaccines (Basel). 2021;9(9):965. doi:10.3390/vaccines9090965.
  • Hughes MM, Reed C, Flannery B, et al. Projected population benefit of increased effectiveness and coverage of influenza vaccination on influenza burden in the United States. Clin Infect Dis. 2020;70(12):2496–2502. doi:10.1093/cid/ciz676.
  • Hohmann E, Brand JC, Rossi MJ, et al. Expert opinion is necessary: delphi panel methodology facilitates a scientific approach to consensus. Arthroscopy. 2018;34(2):349–351. doi:10.1016/j.arthro.2017.11.022.