Effectiveness and harms of seasonal and pandemic influenza vaccines in children, adults and elderly: A critical review and re-analysis of 15 meta-analyses

Human Vaccines and Immunotherapeutics

Volumn 8, Issue 7, 2012, Pages 851-862

  Manzoli, Lamberto ^a   Ioannidis, John P A ^b   Flacco, Maria Elena ^a   De Vito, Corrado ^c   Villari, Paolo ^c  

^a UNIVERSITY OF CHIETI   (Italy)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Influenza vaccine; Meta analysis; Vaccine efficacy; Vaccine immunogenicity; Vaccine safety

Indexed keywords

ADJUVANT; AEROSOL INACTIVATED VACCINE; ALUMINUM; INACTIVATED VACCINE; INFLUENZA VACCINE; LIVE VACCINE; PARENTERAL INACTIVATED VACCINE; PLACEBO; UNCLASSIFIED DRUG; WATER OIL CREAM;

ADULT; AGED; CHILD; DATA ANALYSIS; DRUG EFFICACY; EFFECT SIZE; HUMAN; IMMUNOGENICITY; INFLUENZA; INFLUENZA VACCINATION; META ANALYSIS (TOPIC); OUTCOME ASSESSMENT; PUBLICATION; REVIEW; UNSPECIFIED SIDE EFFECT;

ADULT; AGED; CHILD; DRUG TOXICITY; HUMANS; INFLUENZA VACCINES; INFLUENZA, HUMAN;

EID: 84864071127     PISSN: None     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.19917     Document Type: Review

References (61)

1. Gross PA, Hermogenes AW, Sacks HS, Lau J, Levandowski RA. The efficacy of influenza vaccine in elderly persons. A meta-analysis and review of the literature. Ann Intern Med 1995; 123:518-27; PMID:7661497.
2. Jefferson T, Di Pietrantonj C, Rivetti A, Bawazeer GA, Al-Ansary LA, Ferroni E. Vaccines for preventing influenza in healthy adults. Cochrane Database Syst Rev 2010; CD001269; PMID:20614424.
3. Jefferson T, Di Pietrantonj C, Al-Ansary LA, Ferroni E, Thorning S, Thomas RE. Vaccines for preventing influenza in the elderly. Cochrane Database Syst Rev 2010; CD004876; PMID:20166072.
4. Jefferson T, Rivetti A, Harnden A, Di Pietrantonj C, Demicheli V. Vaccines for preventing influenza in healthy children. Cochrane Database Syst Rev 2008; CD004879; PMID:18425905.
5. Manzoli L, De Vito C, Salanti G, D'Addario M, Villari P, Ioannidis JP. Meta-analysis of the immunogenicity and tolerability of pandemic influenza A 2009 (H1N1) vaccines. PLoS One 2011; 6:e24384.http://dx.doi.org/10.1371/journal. pone.0024384; PMID:21915319
6. Manzoli L, Salanti G, De Vito C, Boccia A, Ioannidis JP, Villari P. Immunogenicity and adverse events of avian influenza A H5N1 vaccine in healthy adults: multiple-treatments meta-analysis. Lancet Infect Dis 2009; 9:482-92.http://dx.doi.org/10.1016/S1473-3099(09)70153-7; PMID:19628173
7. Manzoli L, Schioppa F, Boccia A, Villari P. The efficacy of influenza vaccine for healthy children: a metaanalysis evaluating potential sources of variation in efficacy estimates including study quality. Pediatr Infect Dis J 2007; 26:97-106.http://dx.doi.org/10.1097/01.inf.0000253053.01151.bd; PMID:17259870 (Pubitemid 46183358)
8. Negri E, Colombo C, Giordano L, Groth N, Apolone G, La Vecchia C. Influenza vaccine in healthy children: a meta-analysis. Vaccine 2005; 23:2851-61. http://dx.doi.org/10.1016/j.vaccine.2004.11.053; PMID:15780733 (Pubitemid 40386486)
9. Osterholm MT, Kelley NS, Sommer A, Belongia EA. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 2011; 12:36-44. PMID:22032844.
10. Prieto-Lara E, Llanos-Méndez A. Safety and immunogenicity of prepandemic H5N1 influenza vaccines: a systematic review of the literature. Vaccine 2010; 28:4328-34.http://dx.doi.org/10.1016/j.vaccine.2010.03.068; PMID:20403350
11. Puig Barberà J, Márquez Calderón S. [Effectiveness of influenza vaccine in the elderly. A critical review of the bibliography]. Med Clin (Barc) 1995; 105:645-8; PMID:8558962.
12. Rhorer J, Ambrose CS, Dickinson S, Hamilton H, Oleka NA, Malinoski FJ, et al. Efficacy of live attenuated influenza vaccine in children: A meta-analysis of nine randomized clinical trials. Vaccine 2009; 27:1101-10.http://dx.doi.org/ 10.1016/j.vaccine.2008.11.093; PMID:19095024
13. Villari P, Manzoli L, Boccia A. Methodological quality of studies and patient age as major sources of variation in efficacy estimates of influenza vaccination in healthy adults: a meta-analysis. Vaccine 2004; 22:3475-86. http://dx.doi.org/10.1016/j.vaccine.2004.01.068; PMID:15308375 (Pubitemid 39078767)
14. Vu T, Farish S, Jenkins M, Kelly H. A meta-analysis of effectiveness of influenza vaccine in persons aged 65 years and over living in the community. Vaccine 2002; 20:1831-6.http://dx.doi.org/10.1016/S0264-410X(02)00041-5; PMID:11906772 (Pubitemid 34242840)
15. Yin JK, Khandaker G, Rashid H, Heron L, Ridda I, Booy R. Immunogenicity and safety of pandemic influenza A (H1N1) 2009 vaccine: systematic review and meta-analysis. Influenza Other Respi Viruses 2011; 5:299-305.http://dx.doi.org/ 10.1111/j.1750-2659.2011.00229.x; PMID:21668694
16. Centers for Disease Control and Prevention. Prevention and control of seasonal influenza with vaccines. Recommendations of the Advisory Committee on Immunization Practices (ACIP). Morbidity and Mortality Weekly Report 2009; 58(RR-8).
17. Ioannidis JP. Integration of evidence from multiple meta-analyses: a primer on umbrella reviews, treatment networks and multiple treatments meta-analyses. CMAJ 2009; 181:488-93.http://dx.doi.org/10.1503/cmaj.081086; PMID:19654195
18. Kelly H, Valenciano M. Estimating the effect of influenza vaccines. Lancet Infect Dis 2011; 12:5-6. PMID:22032845.
19. Last JM, ed. A dictionary of epidemiology, 4th edn. New York: Oxford University Press, 2001.
20. Beyer WE, de Bruijn IA, Palache AM, Westendorp RG, Osterhaus AD. Protection against influenza after annually repeated vaccination: a meta-analysis of serologic and field studies. Arch Intern Med 1999; 159:182-8.http://dx.doi.org/10.1001/archinte.159.2.182; PMID:9927102 (Pubitemid 29055107)
21. Beyer WE, Palache AM, Kerstens R, Masurel N. Gender differences in local and systemic reactions to inactivated influenza vaccine, established by a meta-analysis of fourteen independent studies. Eur J Clin Microbiol Infect Dis 1996; 15:65-70.http://dx.doi.org/10.1007/BF01586187; PMID:8641306 (Pubitemid 26051264)
22. Beyer WE, Palache AM, Osterhaus AD. Comparison of Serology and Reactogenicity between Influenza Subunit Vaccines and Whole Virus or Split Vaccines: A Review and Meta-Analysis of the Literature. Clin Drug Investig 1998; 15:1-12.http://dx.doi.org/10.2165/00044011-199815010-00001; PMID:18370460 (Pubitemid 28073487)
23. Pedersen AF, Zachariae R, Bovbjerg DH. Psychological stress and antibody response to influenza vaccination: a meta-analysis. Brain Behav Immun 2009; 23:427-33.http://dx.doi.org/10.1016/j.bbi.2009.01.004; PMID:19486657
24. De Vito C, Manzoli L, Marzuillo C, Anastasi D, Boccia A, Villari P. A systematic review evaluating the potential for bias and the methodological quality of meta-analyses in vaccinology. Vaccine 2007; 25:8794-806.http://dx. doi.org/10.1016/j.vaccine.2007.10.034; PMID:18035456 (Pubitemid 350192058)
25. Lau JI, Ioannidis JP, Schmid CH. Quantitative synthesis in systematic reviews. Ann Intern Med 1997;127:820-6; PMID:9382404.
26. Ioannidis JP, Patsopoulos NA, Evangelou E. Uncertainty in heterogeneity estimates in meta-analyses. BMJ 2007; 335:914-6.http://dx.doi.org/10.1136/bmj. 39343.408449.80; PMID:17974687 (Pubitemid 350076978)
27. Jefferson T, Smith S, Demicheli V, Harnden A, Rivetti A. Safety of influenza vaccines in children. Lancet 2005; 366:803-4.http://dx.doi.org/10. 1016/S0140-6736(05)67204-2; PMID:16139646
28. Ozgur SK, Beyazova U, Kemaloglu YK, Maral I, Sahin F, Camurdan AD, et al. Effectiveness of inactivated influenza vaccine for prevention of otitis media in children. Pediatr Infect Dis J 2006; 25:401-4.http://dx.doi.org/10.1097/01. inf.0000217370.83948.51; PMID:16645502
29. Block SL, Heikkinen T, Toback SL, Zheng W, Ambrose CS. The efficacy of live attenuated influenza vaccine against influenza-associated acute otitis media in children. Pediatr Infect Dis J 2011; 30:203-7. http://dx.doi.org/10. 1097/INF.0b013e3181faac7c; PMID:20935591
30. Beyer WE, Nauta JJ, Palache AM, Giezeman KM, Osterhaus AD. Immunogenicity and safety of inactivated influenza vaccines in primed populations: a systematic literature review and meta-analysis. Vaccine 2011; 29:5785-92.http://dx.doi.org/10.1016/j.vaccine. 2011.05.040; PMID:21624411
31. Ioannidis JP, Chew P, Lau J. Standardized retrieval of side effects data for meta-analysis of safety outcomes. A feasibility study in acute sinusitis. J Clin Epidemiol 2002; 55:619-26.http://dx.doi.org/10.1016/S0895-4356(02)00393-1; PMID:12063104 (Pubitemid 34621506)
32. Ambrose CS, Yi T, Falloon J. An integrated, multi-study analysis of the safety of Ann Arbor strain live attenuated influenza vaccine in children aged 2-17 years. Influenza Other Respi Viruses 2011; 5:389-97. http://dx.doi.org/10. 1111/j.1750-2659.2011.00243.x; PMID:21668683
33. Centers for Disease Control and Prevention (CDC). Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2011. MMWR Morb Mortal Wkly Rep 2011; 60:1128-32; PMID:21866086.
34. Salvadori MI. Influenza vaccine recommendations for children and youth for the 2011/2012 season. Paediatr Child Health (Oxford) 2011; 16:570-1.
35. Jackson LA, Gaglani MJ, Keyserling HL, Balser J, Bouveret N, Fries L, et al. 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;10:71.http://dx.doi.org/10.1186/1471-2334-10-71; PMID:20236548
36. Monto AS, Ohmit SE, Petrie JG, Johnson E, Truscon R, Teich E, et al. Comparative efficacy of inactivated and live attenuated influenza vaccines. N Engl J Med 2009; 361:1260-7.http://dx.doi.org/10.1056/NEJMoa0808652; PMID:19776407
37. Ohmit SE, Victor JC, Rotthoff JR, Teich ER, Truscon RK, Baum LL, et al. Prevention of antigenically drifted influenza by inactivated and live attenuated vaccines. N Engl J Med 2006; 355:2513-22.http://dx.doi.org/10.1056/ NEJMoa061850; PMID:17167134 (Pubitemid 44917499)
38. Ohmit SE, Victor JC, Teich ER, Truscon RK, Rotthoff JR, Newton DW, et al. Prevention of symptomatic seasonal influenza in 2005-2006 by inactivated and live attenuated vaccines. J Infect Dis 2008; 198:312-7. http://dx.doi.org/10. 1086/589885; PMID:18522501
39. Petrie JG, Ohmit SE, Johnson E, Cross RT, Monto AS. Efficacy studies of influenza vaccines: effect of end points used and characteristics of vaccine failures. J Infect Dis 2011; 203:1309-15.http://dx.doi.org/10.1093/infdis/ jir015; PMID:21378375
40. Lasky T, Terracciano GJ, Magder L, Koski CL, Ballesteros M, Nash D, et al. The Guillain-Barré syndrome and the 1992-1993 and 1993-1994 influenza vaccines. N Engl J Med 1998; 339:1797-802. http://dx.doi.org/10.1056/ NEJM199812173392501; PMID:9854114 (Pubitemid 29005783)
41. Banzhoff A, Nacci P, Podda A. A new MF59-adjuvanted influenza vaccine enhances the immune response in the elderly with chronic diseases: results from an immunogenicity meta-analysis. Gerontology 2003;49:177-84.http://dx.doi.org/ 10.1159/000069172; PMID:12679609 (Pubitemid 36438758)
42. van Essen GA, Palache AM, Forleo E, Fedson DS. Influenza vaccination in 2000: recommendations and vaccine use in 50 developed and rapidly developing countries. Vaccine 2003; 21:1780-5. http://dx.doi.org/10.1016/S0264-410X(03) 00072-0; PMID:12686094 (Pubitemid 36398373)
43. Rudenko LG, Arden NH, Grigorieva E, Naychin A, Rekstin A, Klimov AI, et al. Immunogenicity and efficacy of Russian live attenuated and US inactivated influenza vaccines used alone and in combination in nursing home residents. Vaccine 2000; 19:308-18. http://dx.doi.org/10.1016/S0264-410X(00)00153-5; PMID:10930686 (Pubitemid 30621525)
44. Edmondson WP Jr., Rothenberg R, White PW, Gwaltney JM Jr. A comparison of subcutaneous, nasal, and combined influenza vaccination. II. Protection against natural challenge. Am J Epidemiol 1971;93:480-6; PMID:5562720.
45. Liu WM, van der Zeijst BA, Boog CJ, Soethout EC. Aging and impaired immunity to influenza viruses: implications for vaccine development. Hum Vaccin 2011; 7(Suppl):94-8.http://dx.doi.org/10.4161/hv.7.0.14568; PMID:21301210
46. Stuart WH, Dull HB, Newton LH, McQueen JL, Schiff ER. Evaluation of monovalent influenza vaccine in a retirement community during the epidemic of 1965-66. JAMA 1969; 209:232-8.http://dx.doi.org/10.1001/jama.1969. 03160150018005; PMID:5819227
47. Simonsen L, Reichert TA, Viboud C, Blackwelder WC, Taylor RJ, Miller MA. Impact of influenza vaccination on seasonal mortality in the US elderly population. Arch Intern Med 2005; 165:265-72.http://dx.doi.org/10.1001/archinte. 165.3.265; PMID:15710788 (Pubitemid 40216277)
48. Allsup S, Haycox A, Regan M, Gosney M. Is influenza vaccination cost effective for healthy people between ages 65 and 74 years? A randomised controlled trial. Vaccine 2004; 23:639-45; PMID:15542184.
49. Belongia EA, Kieke BA, Donahue JG, Greenlee RT, Balish A, Foust A, et al.; Marshfield Influenza Study Group. Effectiveness of inactivated influenza vaccines varied substantially with antigenic match from the 2004-2005 season to the 2006-2007 season. J Infect Dis 2009; 199:159-67.http://dx.doi.org/10.1086/ 595861; PMID:19086915
50. Dean AS, Moffatt CR, Rosewell A, Dwyer DE, Lindley RI, Booy R, et al. Incompletely matched influenza vaccine still provides protection in frail elderly. Vaccine 2010; 28:864-7.http://dx.doi.org/10.1016/j.vaccine.2009.03.024; PMID:19931952
51. Jackson LA, Jackson ML, Nelson JC, Neuzil KM, Weiss NS. Evidence of bias in estimates of influenza vaccine effectiveness in seniors. Int J Epidemiol 2006;35:337-44.http://dx.doi.org/10.1093/ije/dyi274; PMID:16368725
52. Siontis GC, Ioannidis JP. Risk factors and interventions with statistically significant tiny effects. Int J Epidemiol 2011; 40:1292-307.http://dx.doi.org/10.1093/ije/dyr099; PMID:21737403
53. Salanti G, Higgins JP, Ades AE, Ioannidis JP. Evaluation of networks of randomized trials. Stat Methods Med Res 2008; 17:279-301.http://dx.doi.org/10. 1177/0962280207080643; PMID:17925316
54. Valenciano M, Kissling E, Cohen JM, Oroszi B, Barret AS, Rizzo C, et al. Estimates of pandemic influenza vaccine effectiveness in Europe, 2009-2010: results of Influenza Monitoring Vaccine Effectiveness in Europe (I-MOVE) multicentre case-control study. PLoS Med 2011; 8:e1000388.http://dx.doi.org/10. 1371/journal.pmed.1000388; PMID:21379316
55. Wu J, Xu F, Lu L, Lu M, Miao L, Gao T, et al. Safety and effectiveness of a 2009 H1N1 vaccine in Beijing. N Engl J Med 2010; 363:2416-23.http://dx.doi. org/10.1056/NEJMoa1006736; PMID:21158658
56. Mahmud S, Hammond G, Elliott L, Hilderman T, Kurbis C, Caetano P, et al. Effectiveness of the pandemic H1N1 influenza vaccines against laboratoryconfirmed H1N1 infections: population-based casecontrol study. Vaccine 2011; 29:7975-81.http://dx.doi. org/10.1016/j.vaccine.2011.08.068; PMID:21884747
57. Prosser LA, Lavelle TA, Fiore AE, Bridges CB, Reed C, Jain S, et al. Cost-effectiveness of 2009 pandemic influenza A(H1N1) vaccination in the United States. PLoS One 2011; 6:e22308.http://dx.doi.org/10.1371/journal.pone.0022308; PMID:21829456
58. Ioannidis JP, Manzoli L, De Vito C, D'Addario M, Villari P. Publication delay of randomized trials on 2009 influenza A (H1N1) vaccination. PLoS One 2011; 6:e28346.http://dx.doi.org/10.1371/journal. pone.0028346; PMID:22164274
59. Chiatti C, Barbadoro P, Lamura G, Di Stanislao F, Prospero E. Improving the delivery of flu vaccine for the older people in times of economic recession: what social epidemiology tells us, and what else we need to know. Hum Vaccin 2011; 7:986-8.http://dx.doi.org/10.4161/hv.7.9.16693; PMID:21860260
60. Durando P, Iudici R, Alicino C, Alberti M, de Florentis D, Ansaldi F, et al. Adjuvants and alternative routes of administration towards the development of the ideal influenza vaccine. Hum Vaccin 2011; 7(Suppl):29-40.http://dx.doi. org/10.4161/hv.7.0.14560; PMID:21245655
61. Beran J, Wertzova V, Honegr K, Kaliskova E, Havlickova M, Havlik J, et al. Challenge of conducting a placebo-controlled randomized efficacy study for influenza vaccine in a season with low attack rate and a mismatched vaccine B strain: a concrete example. BMC Infect Dis 2009; 9:2.http://dx.doi.org/10.1186/ 1471-2334-9-2; PMID:19149900