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Abstract

Introduction

When influenza vaccination is ineffective in preventing influenza virus infection, it may still reduce the severity of influenza-associated disease. Here, we estimate the effect of influenza vaccination in preventing severe outcomes e.g. intensive care unit (ICU) admission and death, even though it did not prevent influenza virus infection and subsequent hospitalisation.

Methods

An observational case–case epidemiological study was carried out in 12 sentinel hospitals in Catalonia (Spain) over six influenza seasons 2010/11–2015/16. Cases were individuals with severe laboratory-confirmed influenza virus infection and aged 18 years and older. For each reported case we collected demographic, virological and clinical characteristics. Logistic regression was used to estimate the crude, adjusted odd ratios (aOR) and 95% confidence intervals (CI).

Results

Of 1,727 hospitalised patients included in the study, 799 were female (46.7%), 591 (34.2%) were admitted to the ICU and 223 (12.9%) died. Influenza vaccination uptake was lower in cases that required ICU admission or died (21.2% vs 29.7%, p < 0.001). The adjusted influenza vaccination effectiveness in preventing ICU admission or death was 23% (95% CI: 1 to 40). In an analysis restricted to sex, age group and antiviral treatment, influenza vaccination had a positive effect on disease severity in all age groups and categories.

Conclusions

We found that influenza vaccination reduced the severity of disease even in cases where it did not prevent infection and influenza-associated hospitalisation. Therefore, increased vaccination uptake may reduce complications, ICU admission and death.

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/content/10.2807/1560-7917.ES.2018.23.43.1700732
2018-10-25
2024-03-19
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2018.23.43.1700732
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References

  1. World Health Organization (WHO). Influenza (Seasonal). Fact sheet. Geneva: WHO; 2016. Available from: http://www.who.int/mediacentre/factsheets/fs211/en/
  2. World Health Organization (WHO). Global Epidemiological Surveillance Standards for Influenza. Geneva: WHO; 2014. Available from: http://www.who.int/influenza/resources/documents/WHO_Epidemiological_Influenza_Surveillance_Standards_2014.pdf?ua=1
  3. Chaves SS, Aragon D, Bennett N, Cooper T, D’Mello T, Farley M, et al. Patients hospitalized with laboratory-confirmed influenza during the 2010-2011 influenza season: exploring disease severity by virus type and subtype. J Infect Dis. 2013;208(8):1305-14.  https://doi.org/10.1093/infdis/jit316  PMID: 23863950 
  4. Ohmit SE, Thompson MG, Petrie JG, Thaker SN, Jackson ML, Belongia EA, 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.  https://doi.org/10.1093/cid/cit736  PMID: 24235265 
  5. McLean HQ, Thompson MG, Sundaram ME, Kieke BA, Gaglani M, Murthy K, 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):1529-40.  https://doi.org/10.1093/infdis/jiu647  PMID: 25406334 
  6. Kissling E, Valenciano M, Buchholz U, Larrauri A, Cohen JM, Nunes B, et al. Influenza vaccine effectiveness estimates in Europe in a season with three influenza type/subtypes circulating: the I-MOVE multicentre case-control study, influenza season 2012/13. Euro Surveill. 2014;19(6):20701.  https://doi.org/10.2807/1560-7917.ES2014.19.6.20701  PMID: 24556348 
  7. Valenciano M, Kissling E, Reuss A, Rizzo C, Gherasim A, Horváth JK, et al. Joan O’Donell; I-MOVE multicentre case-control team. Vaccine effectiveness in preventing laboratory-confirmed influenza in primary care patients in a season of co-circulation of influenza A(H1N1)pdm09, B and drifted A(H3N2), I-MOVE Multicentre Case-Control Study, Europe 2014/15. Euro Surveill. 2016;21(7):30139.  https://doi.org/10.2807/1560-7917.ES.2016.21.7.30139  PMID: 26924024 
  8. Turner N, Pierse N, Bissielo A, Huang Q, Radke S, Baker M, et al. SHIVERS investigation team. Effectiveness of seasonal trivalent inactivated influenza vaccine in preventing influenza hospitalisations and primary care visits in Auckland, New Zealand, in 2013. Euro Surveill. 2014;19(34):20884.  https://doi.org/10.2807/1560-7917.ES2014.19.34.20884  PMID: 25188614 
  9. Sullivan SG, Cowling BJ, Greenland S. Frailty and influenza vaccine effectiveness. Vaccine. 2016;34(39):4645-6.  https://doi.org/10.1016/j.vaccine.2016.08.003  PMID: 27578296 
  10. Weinberger B, Herndler-Brandstetter D, Schwanninger A, Weiskopf D, Grubeck-Loebenstein B. Biology of immune responses to vaccines in elderly persons. Clin Infect Dis. 2008;46(7):1078-84.  https://doi.org/10.1086/529197  PMID: 18444828 
  11. He XS, Holmes TH, Sanyal M, Albrecht RA, García-Sastre A, Dekker CL, et al. Distinct patterns of B-cell activation and priming by natural influenza virus infection versus inactivated influenza vaccination. J Infect Dis. 2015;211(7):1051-9.  https://doi.org/10.1093/infdis/jiu580  PMID: 25336731 
  12. Gilca R, De Serres G, Boulianne N, Ouhoummane N, Papenburg J, Douville-Fradet M, et al. Risk factors for hospitalization and severe outcomes of 2009 pandemic H1N1 influenza in Quebec, Canada. Influenza Other Respi Viruses. 2011;5(4):247-55.  https://doi.org/10.1111/j.1750-2659.2011.00204.x  PMID: 21651735 
  13. McLean HQ, Meece JK, Belongia EA. Influenza vaccination and risk of hospitalization among adults with laboratory confirmed influenza illness. Vaccine. 2014;32(4):453-7.  https://doi.org/10.1016/j.vaccine.2013.11.060  PMID: 24291201 
  14. Ridenhour BJ, Campitelli MA, Kwong JC, Rosella LC, Armstrong BG, Mangtani P, et al. Effectiveness of inactivated influenza vaccines in preventing influenza-associated deaths and hospitalizations among Ontario residents aged ≥ 65 years: estimates with generalized linear models accounting for healthy vaccinee effects. PLoS One. 2013;8(10):e76318.  https://doi.org/10.1371/journal.pone.0076318  PMID: 24146855 
  15. Hudgens MGMEH, Halloran ME. Causal Vaccine Effects on Binary Postinfection Outcomes. J Am Stat Assoc. 2006;101(473):51-64.  https://doi.org/10.1198/016214505000000970  PMID: 19096723 
  16. Torner N, Martínez A, Basile L, Plasencia E, Barrabeig I, Follia N, et al. Vigilància epidemiològica dels casos greus hospitalitzats confirmats de grip. Xarxa sentinella PIDIRAC (Catalunya 2010-2015) [Epidemiological surveillance of confirmed hospitalized severe cases of flu. PIDIRAC sentinel network (Catalunya 2010-2015)]. Butlletí Epidemiol Catalunya [Epidemiological bulletin of Catalonia]. 2016;37:234-53. [Spanish]. Available from: http://canalsalut.gencat.cat/ca/actualitat/llista_butlletins/salut_publica/butlleti_epidemiologic_de_catalunya/
  17. European Commission. Commission Regulation (EC) No 2018/945 of 22 June 2018 on the communicable diseases and related special health issues to be covered by epidemiological surveillance as well as relevant case definitions. Official Journal of the European Union. 6.7.2018:L 170/1. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32018D0945&from=EN#page=24
  18. The R Project for Statistical Computing (R). The comprehensive R Archive Network. R; 2018. Available from: http://cran.r-project.org
  19. Catania J, Que LG, Govert JA, Hollingsworth JW, Wolfe CR. High intensive care unit admission rate for 2013-2014 influenza is associated with a low rate of vaccination. Am J Respir Crit Care Med. 2014;189(4):485-7.  https://doi.org/10.1164/rccm.201401-0066LE  PMID: 24512430 
  20. Casado I, Domínguez A, Toledo D, Chamorro J, Force L, Soldevila N, et al. Effect of influenza vaccination on the prognosis of hospitalized influenza patients. Expert Rev Vaccines. 2016;15(3):425-32. PMID: 26690376 
  21. Loubet P, Samih-Lenzi N, Galtier F, Vanhems P, Loulergue P, Duval X, et al. Factors associated with poor outcomes among adults hospitalized for influenza in France: A three-year prospective multicenter study. J Clin Virol. 2016;79:68-73.  https://doi.org/10.1016/j.jcv.2016.04.005  PMID: 27105315 
  22. Arriola CS, Anderson EJ, Baumbach J, Bennett N, Bohm S, Hill M, et al. Does influenza vaccination modify influenza severity? Data on older adults hospitalized with influenza during the 2012-2013 season in the United States. J Infect Dis. 2015;212(8):1200-8.  https://doi.org/10.1093/infdis/jiv200  PMID: 25821227 
  23. Castilla J, Navascués A, Fernández-Alonso M, Reina G, Albéniz E, Pozo F, et al. Effects of previous episodes of influenza and vaccination in preventing laboratory-confirmed influenza in Navarre, Spain, 2013/14 season. Euro Surveill. 2016;20(22):30243.  https://doi.org/10.2807/1560-7917.ES.2016.21.22.30243  PMID: 27277013 
  24. Ministerio de Sanidad, Consumo y Bienestar Social. Tabla 13. Evolución de cobertura de vacunación antigripal en población ≥ 65 años. España, temporadas 2008-2009 a 2017-2018. [Table 13. Evolution of coverage of influenza vaccination in population ≥ 65 years. Spain, seasons 2008-2009 to 2017-2018]. Madrid: Gobierno de España [Government of Spain]; 2018. Spanish. Available from: https://www.mscbs.gob.es/profesionales/saludPublica/prevPromocion/vacunaciones/docs/CoberturasVacunacion/Tabla13.pdf
  25. Thomas PG, Keating R, Hulse-Post DJ, Doherty PC. Cell-mediated protection in influenza infection. Emerg Infect Dis. 2006;12(1):48-54.  https://doi.org/10.3201/eid1201.051237  PMID: 16494717 
  26. Tu W, Mao H, Zheng J, Liu Y, Chiu SS, Qin G, et al. Cytotoxic T lymphocytes established by seasonal human influenza cross-react against 2009 pandemic H1N1 influenza virus. J Virol. 2010;84(13):6527-35.  https://doi.org/10.1128/JVI.00519-10  PMID: 20410263 
  27. Skowronski DM, Hottes TS, McElhaney JE, Janjua NZ, Sabaiduc S, Chan T, et al. Immuno-epidemiologic correlates of pandemic H1N1 surveillance observations: higher antibody and lower cell-mediated immune responses with advanced age. J Infect Dis. 2011;203(2):158-67.  https://doi.org/10.1093/infdis/jiq039  PMID: 21288814 
  28. Chan MC, Lee N, Ngai KL, Leung TF, Chan PK. Clinical and virologic factors associated with reduced sensitivity of rapid influenza diagnostic tests in hospitalized elderly patients and young children. J Clin Microbiol. 2014;52(2):497-501.  https://doi.org/10.1128/JCM.02316-13  PMID: 24478479 
  29. Cromer D, van Hoek AJ, Jit M, Edmunds WJ, Fleming D, Miller E. The burden of influenza in England by age and clinical risk group: a statistical analysis to inform vaccine policy. J Infect. 2014;68(4):363-71.  https://doi.org/10.1016/j.jinf.2013.11.013  PMID: 24291062 
  30. Mereckiene J, Cotter S, Nicoll A, Lopalco P, Noori T, Weber J, et al. VENICE project gatekeepers group. Seasonal influenza immunisation in Europe. Overview of recommendations and vaccination coverage for three seasons: pre-pandemic (2008/09), pandemic (2009/10) and post-pandemic (2010/11). Euro Surveill. 2014;19(16):20780.  https://doi.org/10.2807/1560-7917.ES2014.19.16.20780  PMID: 24786262 
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