Comparing influenza vaccine efficacy against mismatched and matched strains: a systematic review and meta-analysis

BMC Medicine

Mark Loeb²  Chris T Bauch⁵  Mariam Tashkandi⁷  Maggie H Chen⁴  Genevieve Meier³  David Hallett¹  Charlene Soobiah⁴  Ayman Chit⁶  Andrea C Tricco⁴ 

[1] Institute of Medical Sciences, University of Toronto, Toronto, Ontario, Canada;Faculty of Health Sciences, McMaster University, Michael G DeGroote Centre for Learning, Hamilton, Ontario, Canada;North America Vaccines Division, GlaxoSmithKline, Philadelphia, PA, USA;Li Ka Shing Knowledge Institute of St Michael’s Hospital, Toronto, Ontario, Canada;Department of Mathematics and Statistics, University of Guelph, Guelph, Ontario, Canada;Faculty of Pharmacy, University of Toronto, Toronto, Ontario, Canada;Applied Health Research Centre, St Michael’s Hospital, Toronto, Ontario, Canada

关键词: Vaccines;    Systematic review;    Meta-analysis;    Influenza B virus;    Influenza A virus;    Cross protection;    Antigenic variation;   

Others  :  856977
DOI  :  10.1186/1741-7015-11-153

 received in 2012-12-06, accepted in 2013-05-21,  发布年份 2013

【 摘 要 】

Background

Influenza vaccines are most effective when the antigens in the vaccine match those of circulating strains. However, antigens contained in the vaccines do not always match circulating strains. In the present work we aimed to examine the vaccine efficacy (VE) afforded by influenza vaccines when they are not well matched to circulating strains.

Methods

We identified randomized clinical trials (RCTs) through MEDLINE, EMBASE, the Cochrane Library, and references of included RCTs. RCTs reporting laboratory-confirmed influenza among healthy participants vaccinated with antigens of matching and non-matching influenza strains were included. Two independent reviewers screened citations/full-text articles, abstracted data, and appraised risk of bias. Conflicts were resolved by discussion. A random effects meta-analysis was conducted. VE was calculated using the following formula: (1 - relative risk × 100%).

Results

We included 34 RCTs, providing data on 47 influenza seasons and 94,821 participants. The live-attenuated influenza vaccine (LAIV) showed significant protection against mismatched (six RCTs, VE 54%, 95% confidence interval (CI) 28% to 71%) and matched (seven RCTs, VE 83%, 95% CI 75% to 88%) influenza strains among children aged 6 to 36 months. Differences were observed between the point estimates for mismatched influenza A (five RCTs, VE 75%, 95% CI 41% to 90%) and mismatched influenza B (five RCTs, VE 42%, 95% CI 22% to 56%) estimates among children aged 6 to 36 months. The trivalent inactivated vaccine (TIV) also afforded significant protection against mismatched (nine RCTs, VE 52%, 95% CI 37% to 63%) and matched (eight RCTs, VE 65%, 95% CI 54% to 73%) influenza strains among adults. Numerical differences were observed between the point estimates for mismatched influenza A (five RCTs, VE 64%, 95% CI 23% to 82%) and mismatched influenza B (eight RCTs, VE 52%, 95% CI 19% to 72%) estimates among adults. Statistical heterogeneity was low (I² <50%) across all meta-analyses, except for the LAIV meta-analyses among children (I² = 79%).

Conclusions

The TIV and LAIV vaccines can provide cross protection against non-matching circulating strains. The point estimates for VE were different for matching versus non-matching strains, with overlapping CIs.

【 授权许可】

   
2013 Tricco et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Fiore AE, Uyeki TM, Broder K, Finelli L, Euler GL, Singleton JA, Iskander JK, Wortley PM, Shay DK, Bresee JS, Cox NJ: Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR Recomm Rep 2010, 59:1-62.
• [2]Osterholm MT, Kelley NS, Sommer A, Belongia EA: Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 2012, 12:36-44.
• [3]Ampofo WK, Baylor N, Cobey S, Cox NJ, Daves S, Edwards S, Ferguson N, Grohmann G, Hay A, Katz J, Kullabutr K, Lambert L, Levandowski R, Mishra AC, Monto A, Siqueira M, Tashiro M, Waddell AL, Wairagkar N, Wood J, Zambon M, Zhang W, WHO Writing Group: Improving influenza vaccine virus selection: report of a WHO informal consultation held at WHO headquarters, Geneva, Switzerland, 14–16 June 2010. Influenza Other Respi Viruses 2012, 6:142-152. e141-145
• [4]Centers for Disease Control and Prevention: Seasonal Influenza (Flu)- Past Weekly Surveillance Reports. Atlanta, GA: Centers for Disease Control and Prevention; 2012. [Book Seasonal Influenza (Flu)- Past Weekly Surveillance Reports]
• [5]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., 2CD004876
• [6]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., 7CD001269
• [7]Jefferson T, Rivetti A, Di Pietrantonj C, Demicheli V, Ferroni E: Vaccines for preventing influenza in healthy children. Cochrane Database Syst Rev 2012., 8CD004879
• [8]Moher D, Liberati A, Tetzlaff J, Altman DG: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009, 339:b2535.
• [9]Tricco AC, Chit A, Hallett D, Soobiah C, Meier G, Chen M, Tashkandi M, Bauch C, Loeb M: Effect of influenza vaccines against mismatched strains: a systematic review protocol. Syst Rev 2012, 1:35. BioMed Central Full Text
• [10]Bracco Neto H, Farhat CK, Tregnaghi MW, Madhi SA, Razmpour A, Palladino G, Small MG, Gruber WC, Forrest BD: Efficacy and safety of 1 and 2 doses of live attenuated influenza vaccine in vaccine-naive children. Pediatr Infect Dis J 2009, 28:365-371.
• [11]Ohmit SE, Victor JC, Rotthoff JR, Teich ER, Truscon RK, Baum LL, Rangarajan B, Newton DW, Boulton ML, Monto AS: Prevention of antigenically drifted influenza by inactivated and live attenuated vaccines. N Engl J Med 2006, 355:2513-2522.
• [12]Treanor JJ, Schiff GM, Hayden FG, Brady RC, Hay CM, Meyer AL, Holden-Wiltse J, Liang H, Gilbert A, Cox M: Safety and immunogenicity of a baculovirus-expressed hemagglutinin influenza vaccine: a randomized controlled trial. JAMA 2007, 297:1577-1582.
• [13]Ohmit SE, Victor JC, Teich ER, Truscon RK, Rotthoff JR, Newton DW, Campbell SA, Boulton ML, Monto AS: Prevention of symptomatic seasonal influenza in 2005-2006 by inactivated and live attenuated vaccines. J Infect Dis 2008, 198:312-317.
• [14]Monto AS, Ohmit SE, Petrie JG, Johnson E, Truscon R, Teich E, Rotthoff J, Boulton M, Victor JC: Comparative efficacy of inactivated and live attenuated influenza vaccines. N Engl J Med 2009, 361:1260-1267.
• [15]Jackson LA, Gaglani MJ, Keyserling HL, Balser J, Bouveret N, Fries L, Treanor JJ: 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. BioMed Central Full Text
• [16]Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, Savovic J, Schulz KF, Weeks L, Sterne JA: The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 2011, 343:d5928.
• [17]Lexchin J, Bero LA, Djulbegovic B, Clark O: Pharmaceutical industry sponsorship and research outcome and quality: systematic review. BMJ 2003, 326:1167-1170.
• [18]American College Health Association: Influenza-like illness case definition. http://www.acha.org/ILI_Project/ILI_case_definition_CDC.pdf webcite
• [19]Shaw MW, Xu X, Li Y, Normand S, Ueki RT, Kunimoto GY, Hall H, Klimov A, Cox NJ, Subbarao K: Reappearance and global spread of variants of influenza B/Victoria/2/87 lineage viruses in the 2000–2001 and 2001–2002 seasons. Virology 2002, 303:1-8.
• [20]Rota PA, Wallis TR, Harmon MW, Rota JS, Kendal AP, Nerome K: Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983. Virology 1990, 175:59-68.
• [21]DerSimonian R, Laird N: Meta-analysis in clinical trials. Controlled Clin Trials 1986, 7:177-188.
• [22]Higgins JP, Thompson SG: Quantifying heterogeneity in a meta-analysis. Stat Med 2002, 21:1539-1558.
• [23]Egger M, Davey Smith G, Schneider M, Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ 1997, 315:629-634.
• [24]Leibovitz A, Coultrip RL, Kilbourne ED, Legters LJ, Smith CD, Chin J, Schulman JL: Correlated studies of a recombinant influenza-virus vaccine. IV. Protection against naturally occurring influenza in military trainees. J Infect Dis 1971, 124:481-487.
• [25]Beutner KR, Chow T, Rubi E, Strussenberg J, Clement J, Ogra PL: 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, 140:844-850.
• [26]Rytel MW, Jackson LJ, Niebojewski RA, Haagensen JL, Rosenkranz MA: Field trial of live attenuated influenza A/B (“Alice”/R-75) vaccine. Am J Epidemiol 1977, 105:49-55.
• [27]Monto AS, Miller FD, Maassab HF: Evaluation of an attenuated, cold-recombinant influenza B virus vaccine. J Infect Dis 1982, 145:57-64.
• [28]Tannock GA, Bryce DA, Hensley MJ, Saunders NA, Gillett RS, Kennedy WS: Responses to one or two doses of a deoxycholate subunit influenza vaccine in a primed population. Vaccine 1984, 2:100-106.
• [29]Keitel WA, Cate TR, Couch RB, Huggins LL, Hess KR: Efficacy of repeated annual immunization with inactivated influenza virus vaccines over a five year period. Vaccine 1997, 15:1114-1122.
• [30]Gruber WC, Taber LH, Glezen WP, Clover RD, Abell TD, Demmler RW, Couch RB: Live attenuated and inactivated influenza vaccine in school-age children. Am J Dis Child 1990, 144:595-600.
• [31]Edwards KM, Dupont WD, Westrich MK, Plummer WD Jr, Palmer PS, Wright PF: A randomized controlled trial of cold-adapted and inactivated vaccines for the prevention of influenza A disease. J Infect Dis 1994, 169:68-76.
• [32]Clover RD, Crawford S, Glezen WP, Taber LH, Matson CC, Couch RB: 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, 163:300-304.
• [33]Govaert TM, Thijs CT, Masurel N, Sprenger MJ, Dinant GJ, Knottnerus JA: The efficacy of influenza vaccination in elderly individuals. A randomized double-blind placebo-controlled trial. JAMA 1994, 272:1661-1665.
• [34]Powers DC, Smith GE, Anderson EL, Kennedy DJ, Hackett CS, Wilkinson BE, Volvovitz F, Belshe RB, Treanor JJ: Influenza A virus vaccines containing purified recombinant H3 hemagglutinin are well tolerated and induce protective immune responses in healthy adults. J Infect Dis 1995, 171:1595-1599.
• [35]Belshe RB, Mendelman PM, Treanor J, King J, Gruber WC, Piedra P, Bernstein DI, Hayden FG, Kotloff K, Zangwill K, Iacuzio D, Wolff M: The efficacy of live attenuated, cold-adapted, trivalent, intranasal influenzavirus vaccine in children. N Engl J Med 1998, 338:1405-1412.
• [36]Rudenko LG, Arden NH, Grigorieva E, Naychin A, Rekstin A, Klimov AI, Donina S, Desheva J, Holman RC, DeGuzman A, Cox NJ, Katz JM: Immunogenicity and efficacy of Russian live attenuated and US inactivated influenza vaccines used alone and in combination in nursing home residents. Vaccine 2001, 19:308-318.
• [37]Belshe RB, Gruber WC, Mendelman PM, Cho I, Reisinger K, Block SL, Wittes J, Iacuzio D, Piedra P, Treanor J, King J, Kotloff K, Bernstein DI, Hayden FG, Zangwill K, Yan L, Wolff M: 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, 136:168-175.
• [38]Bridges CB, Thompson WW, Meltzer MI, Reeve GR, Talamonti WJ, Cox NJ, Lilac HA, Hall H, Klimov A, Fukuda K: Effectiveness and cost-benefit of influenza vaccination of healthy working adults: a randomized controlled trial. JAMA 2000, 284:1655-1663.
• [39]Hoberman A, Greenberg DP, Paradise JL, Rockette HE, Lave JR, Kearney DH, Colborn DK, Kurs-Lasky M, Haralam MA, Byers CJ, Zoffel LM, Fabian IA, Bernard BS, Kerr JD: Effectiveness of inactivated influenza vaccine in preventing acute otitis media in young children: a randomized controlled trial. JAMA 2003, 290:1608-1616.
• [40]Tam JS, Capeding MR, Lum LC, Chotpitayasunondh T, Jiang Z, Huang LM, Lee BW, Qian Y, Samakoses R, Lolekha S, Rajamohanan KP, Narayanan SN, Kirubakaran C, Rappaport R, Razmpour A, Gruber WC, Forrest BD, Pan-Asian CAIV-T Pediatric Efficacy Trial Network: 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, 26:619-628.
• [41]Vesikari T, Fleming DM, Aristegui JF, Vertruyen A, Ashkenazi S, Rappaport R, Skinner J, Saville MK, Gruber WC, Forrest BD: Safety, efficacy, and effectiveness of cold-adapted influenza vaccine-trivalent against community-acquired, culture-confirmed influenza in young children attending day care. Pediatrics 2006, 118:2298-2312.
• [42]Forrest BD, Pride MW, Dunning AJ, Capeding MR, Chotpitayasunondh T, Tam JS, Rappaport R, Eldridge JH, Gruber WC: Correlation of cellular immune responses with protection against culture-confirmed influenza virus in young children. Clin Vaccine Immunol 2008, 15:1042-1053.
• [43]Lum LC, Borja-Tabora CF, Breiman RF, Vesikari T, Sablan BP, Chay OM, Tantracheewathorn T, Schmitt HJ, Lau YL, Bowonkiratikachorn P, Tam JS, Lee BW, Tan KK, Pejcz J, Cha S, Gutierrez-Brito M, Kaltenis P, Vertruyen A, Czajka H, Bojarskas J, Brooks WA, Cheng SM, Rappaport R, Baker S, Gruber WC, Forrest BD: Influenza vaccine concurrently administered with a combination measles, mumps, and rubella vaccine to young children. Vaccine 2010, 28:1566-1574.
• [44]Langley JM, Aoki F, Ward BJ, McGeer A, Angel JB, Stiver G, Gorfinkel I, Shu D, White L, Lasko B, Dzongowski P, Papp K, Alexander M, Boivin G, Fries L: A nasally administered trivalent inactivated influenza vaccine is well tolerated, stimulates both mucosal and systemic immunity, and potentially protects against influenza illness. Vaccine 2011, 29:1921-1928.
• [45]Beran J, Wertzova V, Honegr K, Kaliskova E, Havlickova M, Havlik J, Jirincova H, Van Belle P, Jain V, Innis B, Devaster JM: 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. BioMed Central Full Text
• [46]Beran J, Vesikari T, Wertzova V, Karvonen A, Honegr K, Lindblad N, Van Belle P, Peeters M, Innis BL, Devaster JM: Efficacy of inactivated split-virus influenza vaccine against culture-confirmed influenza in healthy adults: a prospective, randomized, placebo-controlled trial. J Infect Dis 2009, 200:1861-1869.
• [47]Frey S, Vesikari T, Szymczakiewicz-Multanowska A, Lattanzi M, Izu A, Groth N, Holmes S: Clinical efficacy of cell culture-derived and egg-derived inactivated subunit influenza vaccines in healthy adults. Clinical Infect Dis 2010, 51:997-1004.
• [48]Treanor JJ, El Sahly H, King J, Graham I, Izikson R, Kohberger R, Patriarca P, Cox M: Protective efficacy of a trivalent recombinant hemagglutinin protein vaccine (FluBlok(R)) against influenza in healthy adults: a randomized, placebo-controlled trial. Vaccine 2011, 29:7733-7739.
• [49]Barrett PN, Berezuk G, Fritsch S, Aichinger G, Hart MK, El-Amin W, Kistner O, Ehrlich HJ: Efficacy, safety, and immunogenicity of a Vero-cell-culture-derived trivalent influenza vaccine: a multicentre, double-blind, randomised, placebo-controlled trial. Lancet 2011, 377:751-759.
• [50]Cowling BJ, Ng S, Ma ES, Cheng CK, Wai W, Fang VJ, Chan KH, Ip DK, Chiu SS, Peiris JS, Leung GM: Protective efficacy of seasonal influenza vaccination against seasonal and pandemic influenza virus infection during 2009 in Hong Kong. Clinical Infect Dis 2010, 51:1370-1379.
• [51]Talaat KR, Greenberg ME, Lai MH, Hartel GF, Wichems CH, Rockman S, Jeanfreau RJ, Ghosh MR, Kabongo ML, Gittleson C, Karron RA: A single dose of unadjuvanted novel 2009 H1N1 vaccine is immunogenic and well tolerated in young and elderly adults. J Infect Dis 2010, 202:1327-1337.
• [52]Keitel WA, Cate TR, Couch RB: Efficacy of sequential annual vaccination with inactivated influenza virus vaccine. Am J Epidemiol 1988, 127:353-364.
• [53]Kelly HA, Sullivan SG, Grant KA, Fielding JE: Moderate influenza vaccine effectiveness with variable effectiveness by match between circulating and vaccine strains in Australian adults aged 20–64 years, 2007–2011. Influenza Other Respi Virusesin press
• [54]Landry ML: Diagnostic tests for influenza infection. Curr Opin Pediatr 2011, 23:91-97.
• [55]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, 203:1309-1315.
• [56]Schulz KF, Altman DG, Moher D: CONSORT 2010 Statement: Updated guidelines for reporting parallel group randomised trials. J Clin Epidemiol 2010, 63:834-840.
• [57]Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, Fouchier RA: Mapping the antigenic and genetic evolution of influenza virus. Science 2004, 305:371-376.
• [58]Skowronski DM, Janjua NZ, De Serres G, Winter AL, Dickinson JA, Gardy JL, Gubbay J, Fonseca K, Charest H, Crowcroft NS, Fradet MD, Bastien N, Li Y, Krajden M, Sabaiduc S, Petric M: A sentinel platform to evaluate influenza vaccine effectiveness and new variant circulation, Canada 2010–2011 season. Clinical Infect Dis 2012, 55:332-342.
• [59]Belshe RB, Coelingh K, Ambrose CS, Woo JC, Wu X: Efficacy of live attenuated influenza vaccine in children against influenza B viruses by lineage and antigenic similarity. Vaccine 2012, 28:2149-2156.