Seasonal influenza vaccine efficacy and its determinants in children and non-elderly adults: A systematic review with meta-analyses of controlled trials

Vaccine

Volumn 31, Issue 1, 2012, Pages 49-57

  DiazGranados, Carlos A ^a   Denis, Martine ^a   Plotkin, Stanley ^b  

^a SANOFI PASTEUR   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Influenza vaccines; Meta analysis; Prevention and control; Treatment outcome

Indexed keywords

INFLUENZA VACCINE; LIVE VACCINE;

DRUG EFFICACY; EMBASE; HUMAN; INFLUENZA A; INFLUENZA B; MEDLINE; META ANALYSIS; PRIORITY JOURNAL; REVIEW; SEASONAL INFLUENZA; SYSTEMATIC REVIEW; VACCINATION; VIRUS STRAIN;

ADOLESCENT; ADULT; CHILD; CONTROLLED CLINICAL TRIALS AS TOPIC; FEMALE; HUMANS; INFLUENZA VACCINES; INFLUENZA, HUMAN; MALE; MIDDLE AGED; YOUNG ADULT;

EID: 84870540638     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2012.10.084     Document Type: Review

References (64)

1. Palache A. Seasonal influenza vaccine provision in 157 countries (2004-2009) and the potential influence of national public health policies. Vaccine 2011, 29(51):9459-9466.
2. Thompson W.W., Shay D.K., Weintraub E., Brammer L., Cox N., Anderson L.J., et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003, 289(2):179-186.
3. Thompson W.W., Shay D.K., Weintraub E., Brammer L., Bridges C.B., Cox N.J., et al. Influenza-associated hospitalizations in the United States. JAMA 2004, 292(11):1333-1340.
4. Fiore A.E., Uyeki T.M., Broder K., Finelli L., Euler G.L., Singleton J.A., et al. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR Recomm Rep 2010, 59(RR-8):1-62.
5. Molinari N.A., Ortega-Sanchez I.R., Messonnier M.L., Thompson W.W., Wortley P.M., Weintraub E., et al. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 2007, 25(27):5086-5096.
6. Szucs T. The socio-economic burden of influenza. J Antimicrob Chemother 1999, 44(Suppl. B):11-15.
7. 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.
8. Jackson L.A., Gaglani M.J., Keyserling H.L., 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.
9. Petrie J.G., Ohmit S.E., Johnson E., Cross R.T., Monto A.S. Efficacy studies of influenza vaccines: effect of end points used and characteristics of vaccine failures. J Infect Dis 2011, 203(9):1309-1315.
10. Osterholm M.T., Kelley N.S., Sommer A., Belongia E.A. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 2012, 12(1):36-44.
11. Cochrane Collaboration. Glossary available at: [accessed: 8.10.2012]. http://www.cochrane.org/glossary.
12. Jadad A.R., Moore R.A., Carroll D., Jenkinson C., Reynolds D.J., Gavaghan D.J., et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary?. Control Clin Trials 1996, 17(1):1-12.
13. Sterne J.A.C., Egger M., Davey-Smith G. Investigating and dealing with publication and other biases in meta-analysis. BMJ 2001, 323:101-105.
14. Mantel N., Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959, 22(4):719-748.
15. Beran J., Vesikari T., Wertzova V., Karvonen A., Honegr K., Lindblad N., et al. Efficacy of inactivated split-virus influenza vaccine against culture-confirmed influenza in healthy adults: a prospective, randomized, placebo-controlled trial. J Infect Dis 2009, 200(12):1861-1869.
16. Edwards K.M., Dupont W.D., Westrich M.K., Plummer W.D., Palmer P.S., Wright P.F. A randomized controlled trial of cold-adapted and inactivated vaccines for the prevention of influenza A disease. J Infect Dis 1994, 169(1):68-76.
17. Keitel W.A., Cate T.R., Couch R.B., Huggins L.L., Hess K.R. Efficacy of repeated annual immunization with inactivated influenza virus vaccines over a five year period. Vaccine 1997, 15(10):1114-1122.
18. Monto A.S., Ohmit S.E., Petrie J.G., Johnson E., Truscon R., Teich E., et al. Comparative efficacy of inactivated and live attenuated influenza vaccines. N Engl J Med 2009, 361(13):1260-1267.
19. Ohmit S.E., Victor J.C., Teich E.R., Truscon R.K., Rotthoff J.R., Newton D.W., et al. Prevention of symptomatic seasonal influenza in 2005-2006 by inactivated and live attenuated vaccines. J Infect Dis 2008, 198(3):312-317.
20. Ohmit S.E., Victor J.C., Rotthoff J.R., Teich E.R., Truscon R.K., Baum L.L., et al. Prevention of antigenically drifted influenza by inactivated and live attenuated vaccines. N Engl J Med 2006, 355(24):2513-2522.
21. Spencer M.J., Cherry J.D., Powell K.R., Sumaya C.V., Garakian A.J. Clinical trials with Alice strain, live, attenuated, serum inhibitor-resistant intranasal influenza A vaccine. J Infect Dis 1975, 132(4):415-420.
22. Belshe R.B., Gruber W.C., Mendelman P.M., Cho I., Reisinger K., Block S.L., et al. Efficacy of vaccination with live attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine against a variant (A/Sydney) not contained in the vaccine. J Pediatr 2000, 136(2):168-175.
23. Belshe R.B., Mendelman P.M., Treanor J., King J., Gruber W.C., Piedra P., et al. The efficacy of live attenuated, cold-adapted, trivalent, intranasal influenzavirus vaccine in children. N Engl J Med 1998, 338(20):1405-1412.
24. Gruber W.C., Belshe R.B., King J.C., Treanor J.J., Piedra P.A., Wright P.F., et al. Evaluation of live attenuated influenza vaccines in children 6-18 months of age: safety, immunogenicity, and efficacy. National Institute of Allergy and Infectious Diseases, Vaccine and Treatment Evaluation Program and the Wyeth-Ayerst ca Influenza Vaccine Investigators Group. J Infect Dis 1996, 173(6):1313-1319.
25. Hoberman A., Greenberg D.P., Paradise J.L., Rockette H.E., Lave J.R., Kearney D.H., et al. Effectiveness of inactivated influenza vaccine in preventing acute otitis media in young children: a randomized controlled trial. JAMA 2003, 290(12):1608-1616.
26. Jansen A.G., Sanders E.A., Hoes A.W., van Loon A.M., Hak E. Effects of influenza plus pneumococcal conjugate vaccination versus influenza vaccination alone in preventing respiratory tract infections in children: a randomized, double-blind, placebo-controlled trial. J Pediatr 2008, 153(6):764-770.
27. Andre F.E., Uytterschaut P., Niculescu I.T., Virlan G., Zilisteanu E., Smerdel S., et al. Placebo-controlled double-blind clinical studies on the efficacy of different influenza vaccines assessed by experimental and natural infection. Postgrad Med J 1976, 52(608):352-359.
28. Hammond M.L., Ferris A.A., Faine S., McAvan T. Effective protection against influenza after vaccination with subunit vaccine. Med J Aust 1978, 1(6):301-303.
29. Hoskins T.W., Davies J.R., Allchin A., Miller C.L., Pollock T.M. Controlled trial of inactivated influenza vaccine containing the a-Hong Kong strain during an outbreak of influenza due to the a-England-42-72 strain. Lancet 1973, 2(7821):116-120.
30. Leibovitz A., Coultrip R.L., Kilbourne E.D., Legters L.J., Smith C.D., Chin J., et al. Correlated studies of a recombinant influenza-virus vaccine. IV. Protection against naturally occurring influenza in military trainees. J Infect Dis 1971, 124(5):481-487.
31. Lum L.C., Borja-Tabora C.F., Breiman R.F., Vesikari T., Sablan B.P., Chay O.M., et al. Influenza vaccine concurrently administered with a combination measles, mumps, and rubella vaccine to young children. Vaccine 2010, 28(6):1566-1574.
32. Mair H.J., Sansome D.A., Tillett H.E. A controlled trial of inactivated monovalent influenza A vaccines in general practice. J Hyg (Lond) 1974, 73(2):317-327.
33. Perez Rodriguez A.E., Gonzalez Ochoa E., de Armas Perez L., Goyenechea Hernandez A. Evaluacion de la vacuna antigripal en escolares de secundaria basica. Rev Cubana Med Trop 1989, 41(3):419-434.
34. Rytel M.W., Jackson L.J., Niebojewski R.A., Haagensen J.L., Rosenkranz M.A. Field trial of live attenuated influenza A/B (Alice/R-75) vaccine. Am J Epidemiol 1977, 105(1):49-55.
35. Barrett P.N., Berezuk G., Fritsch S., Aichinger G., Hart M.K., El-Amin W., et al. 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):751-759.
36. Frey S., Vesikari T., Szymczakiewicz-Multanowska A., Lattanzi M., Izu A., Groth N., et al. Clinical efficacy of cell culture-derived and egg-derived inactivated subunit influenza vaccines in healthy adults. Clin Infect Dis 2010, 51(9):997-1004.
37. Tam J.S., Capeding M.R., Lum L.C., Chotpitayasunondh T., Jiang Z., Huang L.M., et al. Efficacy and safety of a live attenuated, cold-adapted influenza vaccine, trivalent against culture-confirmed influenza in young children in Asia. Pediatr Infect Dis J 2007, 26(7):619-628.
38. Vesikari T., Knuf M., Wutzler P., Karvonen A., Kieninger-Baum D., Schmitt H.J., et al. Oil-in-water emulsion adjuvant with influenza vaccine in young children. N Engl J Med 2011, 365(15):1406-1416.
39. Vesikari T., Fleming D.M., Aristegui J.F., Vertruyen A., Ashkenazi S., Rappaport R., et al. Safety, efficacy, and effectiveness of cold-adapted influenza vaccine-trivalent against community-acquired, culture-confirmed influenza in young children attending day care. Pediatrics 2006, 118(6):2298-2312.
40. Powers D.C., Smith G.E., Anderson E.L., Kennedy D.J., Hackett C.S., Wilkinson B.E., et al. Influenza A virus vaccines containing purified recombinant H3 hemagglutinin are well tolerated and induce protective immune responses in healthy adults. J Infect Dis 1995, 171(6):1595-1599.
41. Treanor J.J., Sahly H.E., King J., Graham I., Izikson R., Kohberger R., et al. Protective efficacy of a trivalent recombinant hemagglutinin protein vaccine (FluBlok(R)) against influenza in healthy adults: a randomized, placebo-controlled trial. Vaccine 2011, 29(44):7733-7739.
42. Mogabgab W.J., Leiderman E. Immunogenicity of 1967 polyvalent and 1968 Hong Kong influenza vaccines. JAMA 1970, 211(10):1672-1676.
43. Jefferson T., Di Pietrantonj C., Rivetti A., Bawazeer G.A., Al-Ansary L.A., Ferroni E. Vaccines for preventing influenza in healthy adults. Cochrane Database Syst Rev 2010, (7):CD001269.
44. Jefferson T., Rivetti A., Harnden A., Di Pietrantonj C., Demicheli V. Vaccines for preventing influenza in healthy children. Cochrane Database Syst Rev 2008, D0(2):C04879.
45. Tannock G.A., Bryce D.A., Hensley M.J., Saunders N.A., Gillett R.S., Kennedy W.S. Responses to one or two doses of a deoxycholate subunit influenza vaccine in a primed population. Vaccine 1984, 2(1):100-106.
46. Monto A.S., Miller F.D., Maassab H.F. Evaluation of an attenuated, cold-recombinant influenza B virus vaccine. J Infect Dis 1982, 145(1):57-64.
47. Beutner K.R., Chow T., Rubi E., Strussenberg J., Clement J., Ogra P.L. Evaluation of a neuraminidase-specific influenza A virus vaccine in children: antibody responses and effects on two successive outbreaks of natural infection. J Infect Dis 1979, 140(6):844-850.
48. Keitel W.A., Cate T.R., Couch R.B. Efficacy of sequential annual vaccination with inactivated influenza virus vaccine. Am J Epidemiol 1988, 127(2):353-364.
49. Clover R.D., Crawford S., Glezen W.P., Taber L.H., Matson C.C., Couch R.B. Comparison of heterotypic protection against influenza A/Taiwan/86 (H1N1) by attenuated and inactivated vaccines to A/Chile/83-like viruses. J Infect Dis 1991, 163(2):300-304.
50. De Villiers P.J., Steele A.D., Hiemstra L.A., Rappaport R., Dunning A.J., Gruber W.C., et al. Efficacy and safety of a live attenuated influenza vaccine in adults 60 years of age and older. Vaccine 2009, 28(1):228-234.
51. Treanor J.J., Talbot H.K., Ohmit S.E., Coleman L.A., Thompson M.G., Cheng P.Y., et al. Effectiveness of seasonal influenza vaccines in the United States during a season with circulation of all three vaccine strains. Clin Infect Dis 2012, 55(7):951-959.
52. Engels E.A., Schmid C.H., Terrin N., Olkin I., Lau J. Heterogeneity and statistical significance in meta-analysis: an empirical study of 125 meta-analyses. Stat Med 2000, 19(13):1707-1728.
53. Monto A.S., Maassab H.F. Ether treatment of type B influenza virus antigen for the hemagglutination inhibition test. J Clin Microbiol 1981, 13(1):54-57.
54. Langley J.M., Vanderkooi O.G., Garfield H.A., Hebert J., Chandrasekaran V., Jain V.K., et al. Immunogenicity and safety of 2 dose levels of a thimerosal-free trivalent seasonal influenza vaccine in children aged 6-35 months: a randomized, controlled trial. J Ped Infect Dis 2012, 1(1):55-63.
55. Heckler R., Baillot A., Engelmann H., Neumeier E., Windorfer A. Cross-protection against homologous drift variants of influenza A and B after vaccination with split vaccine. Intervirology 2007, 50(1):58-62.
56. Englund J.A., Walter E.B., Gbadebo A., Monto A.S., Zhu Y., Neuzil K.M. Immunization with trivalent inactivated influenza vaccine in partially immunized toddlers. Pediatrics 2006, 118(3):e579-e585.
57. Ansaldi F., Zancolli M., Durando P., Montomoli E., Sticchi L., Del Giudice G., et al. Antibody response against heterogeneous circulating influenza virus strains elicited by MF59- and non-adjuvanted vaccines during seasons with good or partial matching between vaccine strain and clinical isolates. Vaccine 2010, 28(25):4123-4129.
58. Camilloni B., Neri M., Lepri E., Iorio A.M. Cross-reactive antibodies in middle-aged and elderly volunteers after MF59-adjuvanted subunit trivalent influenza vaccine against B viruses of the B/Victoria or B/Yamagata lineages. Vaccine 2009, 27(31):4099-4103.
59. Belshe R.B. The need for quadrivalent vaccine against seasonal influenza. Vaccine 2010, 28(Suppl. 4):D45-D53.
60. Ashkenazi S., Vertruyen A., Aristegui J., Esposito S., McKeith D.D., Klemola T., et al. Superior relative efficacy of live attenuated influenza vaccine compared with inactivated influenza vaccine in young children with recurrent respiratory tract infections. Pediatr Infect Dis J 2006, 25(10):870-879.
61. Lachenbruch P.A. Sensitivity, specificity, and vaccine efficacy. Control Clin Trials 1998, 19(6):569-574.
62. Forrest B.D., Steele A.D., Hiemstra L., Rappaport R., Ambrose C.S., Gruber W.C. A prospective, randomized, open-label trial comparing the safety and efficacy of trivalent live attenuated and inactivated influenza vaccines in adults 60 years of age and older. Vaccine 2011, 29(20):3633-3639.
63. Govaert T.M., Thijs C.T., Masurel N., Sprenger M.J., Dinant G.J., Knottnerus J.A. The efficacy of influenza vaccination in elderly individuals. A randomized double-blind placebo-controlled trial. JAMA 1994, 272(21):661-665.
64. Praditsuwan R., Assantachai P., Wasi C., Puthavatana P., Kositanont U. The efficacy and effectiveness of influenza vaccination among Thai elderly persons living in the community. J Med Assoc Thai 2005, 88(2):256-264.