Variable influenza vaccine effectiveness by subtype: a systematic review and meta-analysis of test-negative design studies

The Lancet Infectious Diseases

Volumn 16, Issue 8, 2016, Pages 942-951

  Belongia, Edward A ^a   Simpson, Melissa D ^a   King, Jennifer P ^a   Sundaram, Maria E ^b   Kelley, Nicholas S ^b   Osterholm, Michael T ^b   McLean, Huong Q ^a  

^a MARSHFIELD CLINIC   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; LIVE VACCINE; VACCINE;

ARTICLE; CLINICAL EFFECTIVENESS; HUMAN; INFECTION PREVENTION; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); META ANALYSIS; OUTPATIENT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; STUDY DESIGN; SYSTEMATIC REVIEW; VIRUS TYPING; IMMUNOLOGY; INFLUENZA, HUMAN; METHODOLOGY; SENTINEL SURVEILLANCE; VACCINATION;

HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; RESEARCH DESIGN; SENTINEL SURVEILLANCE; VACCINATION; VACCINE POTENCY; VACCINES, ATTENUATED;

EID: 84962635913     PISSN: 14733099     EISSN: 14744457     Source Type: Journal    
DOI: 10.1016/S1473-3099(16)00129-8     Document Type: Article

References (76)

1. 1 Osterholm, MT, Kelley, NS, Sommer, A, Belongia, EA, Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 12 (2012), 36–44.
2. 2 Skowronski, DM, Gilbert, M, Tweed, SA, et al. Effectiveness of vaccine against medical consultation due to laboratory-confirmed influenza: results from a sentinel physician pilot project in British Columbia, 2004–2005. Can Commun Dis Rep 31 (2005), 181–192.
3. 3 Foppa, IM, Haber, M, Ferdinands, JM, Shay, DK, The case test-negative design for studies of the effectiveness of influenza vaccine. Vaccine 31 (2013), 3104–3109.
4. 4 Jackson, ML, Nelson, JC, The test-negative design for estimating influenza vaccine effectiveness. Vaccine 31 (2013), 2165–2168.
5. 5 Katz, JM, Hancock, K, Xu, X, Serologic assays for influenza surveillance, diagnosis and vaccine evaluation. Expert Rev Anti Infect Ther 9 (2011), 669–683.
6. 6 Higgins, JP, Thompson, SG, Quantifying heterogeneity in a meta-analysis. Stat Med 21 (2002), 1539–1558.
7. 7 DerSimonian, R, Laird, N, Meta-analysis in clinical trials. Control Clin Trials 7 (1986), 177–188.
8. 8 Bateman, AC, Kieke, BA, Irving, SA, Meece, JK, Shay, DK, Belongia, EA, Effectiveness of monovalent 2009 pandemic influenza A virus subtype H1N1 and 2010-2011 trivalent inactivated influenza vaccines in Wisconsin during the 2010-2011 influenza season. J Infect Dis 207 (2013), 1262–1269.
9. 9 Belongia, EA, Kieke, BA, Donahue, JG, et al. Influenza vaccine effectiveness in Wisconsin during the 2007–08 season: comparison of interim and final results. Vaccine 29 (2011), 6558–6563.
10. 10 Castilla, J, Martinez-Baz, I, Martinez-Artola, V, et al. Early estimates of influenza vaccine effectiveness in Navarre, Spain: 2012/13 mid-season analysis. Euro Surveill, 18, 2013, 2.
11. 11 Castilla, J, Martinez-Baz, I, Martinez-Artola, V, et al. Decline in influenza vaccine effectiveness with time after vaccination, Navarre, Spain, season 2011/12. Euro Surveill, 18, 2013, 5.
12. 12 Castilla, J, Martinez-Baz, I, Navascues, A, et al. Vaccine effectiveness in preventing laboratory-confirmed influenza in Navarre, Spain: 2013/14 mid-season analysis. Euro Surveill, 19, 2014, 6.
13. 13 Castilla, J, Moran, J, Martinez-Artola, V, et al. Effectiveness of the monovalent influenza A(H1N1)2009 vaccine in Navarre, Spain, 2009–2010: cohort and case-control study. Vaccine 29 (2011), 5919–5924.
14. 14 Englund, H, Campe, H, Hautmann, W, Effectiveness of trivalent and monovalent influenza vaccines against laboratory-confirmed influenza infection in persons with medically attended influenza-like illness in Bavaria, Germany, 2010/2011 season. Epidemiol Infect 141 (2013), 1807–1815.
15. 15 Fielding, JE, Grant, KA, Garcia, K, Kelly, HA, Effectiveness of seasonal influenza vaccine against pandemic (H1N1) 2009 virus, Australia, 2010. Emerg Infect Dis 17 (2011), 1181–1187.
16. 16 Fielding, JE, Grant, KA, Papadakis, G, Kelly, HA, Estimation of type- and subtype-specific influenza vaccine effectiveness in Victoria, Australia using a test negative case control method, 2007–2008. BMC Infect Dis, 11, 2011, 170.
17. 17 Fielding, JE, Grant, KA, Tran, T, Kelly, HA, Moderate influenza vaccine effectiveness in Victoria, Australia, 2011. Euro Surveill, 17, 2012, 11.
18. 18 Flannery, B, Thaker, SN, Clippard, J, et al. Interim estimates of 2013–14 seasonal influenza vaccine effectiveness—United States, February 2014. MMWR Morb Mortal Wkly Rep 63 (2014), 137–142.
19. 19 Fleming, DM, Andrews, NJ, Ellis, JS, et al. Estimating influenza vaccine effectiveness using routinely collected laboratory data. J Epidemiol Community Health 64 (2010), 1062–1067.
20. 20 Griffin, MR, Monto, AS, Belongia, EA, et al. Effectiveness of non-adjuvanted pandemic influenza A vaccines for preventing pandemic influenza acute respiratory illness visits in 4 U.S. communities. PLoS One, 6, 2011, e23085.
21. 21 Hardelid, P, Fleming, DM, McMenamin, J, et al. Effectiveness of pandemic and seasonal influenza vaccine in preventing pandemic influenza A(H1N1)2009 infection in England and Scotland 2009–2010. Euro Surveill, 16, 2011, 2.
22. 22 Janjua, NZ, Skowronski, DM, De Serres, G, et al. Estimates of influenza vaccine effectiveness for 2007–2008 from Canada's sentinel surveillance system: cross-protection against major and minor variants. J Infect Dis 205 (2012), 1858–1868.
23. 23 Jimenez-Jorge, S, Savulescu, C, Pozo, F, et al. Effectiveness of the 2010–11 seasonal trivalent influenza vaccine in Spain: cycEVA study. Vaccine 30 (2012), 3595–3602.
24. 24 Kavanagh, K, Robertson, C, McMenamin, J, Assessment of the variability in influenza A(H1N1) vaccine effectiveness estimates dependent on outcome and methodological approach. PLoS One, 6, 2011, e28743.
25. 25 Kavanagh, K, Robertson, C, McMenamin, J, Estimates of influenza vaccine effectiveness in primary care in Scotland vary with clinical or laboratory endpoint and method—experience across the 2010/11 season. Vaccine 31 (2013), 4556–4563.
26. 26 Kelly, H, Jacoby, P, Dixon, GA, et al. Vaccine effectiveness against laboratory-confirmed influenza in healthy young children: a case-control study. Pediatr Infect Dis J 30 (2011), 107–111.
27. 27 Kissling, E, Valenciano, M, Buchholz, U, 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, 19, 2014, 6.
28. 28 Kissling, E, Valenciano, M, Cohen, JM, et al. I-MOVE multi-centre case control study 2010–11: overall and stratified estimates of influenza vaccine effectiveness in Europe. PLoS One, 6, 2011, e27622.
29. 29 Kissling, E, Valenciano, M, Falcao, J, et al. “I-MOVE” towards monitoring seasonal and pandemic influenza vaccine effectiveness: lessons learnt from a pilot multi-centric case-control study in Europe, 2008–9. Euro Surveill, 14, 2009, 44.
30. 30 Kissling, E, Valenciano, M, Larrauri, A, et al. Low and decreasing vaccine effectiveness against influenza A(H3) in 2011/12 among vaccination target groups in Europe: results from the I-MOVE multicentre case-control study. Euro Surveill, 18, 2013, 5.
31. 31 Lo, YC, Chuang, JH, Kuo, HW, et al. Surveillance and vaccine effectiveness of an influenza epidemic predominated by vaccine-mismatched influenza B/Yamagata-lineage viruses in Taiwan, 2011–12 season. PLoS One, 8, 2013, e58222.
32. 32 Mahmud, S, Hammond, G, Elliott, L, et al. Effectiveness of the pandemic H1N1 influenza vaccines against laboratory-confirmed H1N1 infections: population-based case-control study. Vaccine 29 (2011), 7975–7981.
33. 33 Martinez-Baz, I, Martinez-Artola, V, Reina, G, et al. Effectiveness of the trivalent influenza vaccine in Navarre, Spain, 2010–2011: a population-based test-negative case-control study. BMC Public Health, 13, 2013, 191.
34. 34 Ohmit, SE, Thompson, MG, Petrie, JG, 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 58 (2014), 319–327.
35. 35 Pebody, R, Andrews, N, McMenamin, J, et al. Vaccine effectiveness of 2011/12 trivalent seasonal influenza vaccine in preventing laboratory-confirmed influenza in primary care in the United Kingdom: evidence of waning intra-seasonal protection. Euro Surveill, 18, 2013, 5.
36. 36 Pebody, RG, Andrews, N, Fleming, DM, et al. Age-specific vaccine effectiveness of seasonal 2010/2011 and pandemic influenza A(H1N1) 2009 vaccines in preventing influenza in the United Kingdom. Epidemiol Infect 141 (2013), 620–630.
37. 37 Savulescu, C, Jimenez-Jorge, S, de Mateo, S, et al. Using surveillance data to estimate pandemic vaccine effectiveness against laboratory confirmed influenza A(H1N1)2009 infection: two case-control studies, Spain, season 2009–2010. BMC Public Health, 11, 2011, 899.
38. 38 Savulescu, C, Jimenez-Jorge, S, Delgado-Sanz, C, et al. Higher vaccine effectiveness in seasons with predominant circulation of seasonal influenza A(H1N1) than in A(H3N2) seasons: test-negative case-control studies using surveillance data, Spain, 2003–2011. Vaccine 32 (2014), 4404–4411.
39. 39 Skowronski, DM, De Serres, G, Dickinson, J, et al. Component-specific effectiveness of trivalent influenza vaccine as monitored through a sentinel surveillance network in Canada, 2006–2007. J Infect Dis 199 (2009), 168–179.
40. 40 Skowronski, DM, Janjua, NZ, De Serres, G, et al. Effectiveness of AS03 adjuvanted pandemic H1N1 vaccine: case-control evaluation based on sentinel surveillance system in Canada, autumn 2009. BMJ, 342, 2011, c7297.
41. 41 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, 9, 2014, e92153.
42. 42 Skowronski, DM, Janjua, NZ, De Serres, G, et al. A sentinel platform to evaluate influenza vaccine effectiveness and new variant circulation, Canada 2010-2011 season. Clin Infect Dis 55 (2012), 332–342.
43. 43 Skowronski, DM, Janjua, NZ, Sabaiduc, S, et al. Influenza A/subtype and B/lineage effectiveness estimates for the 2011–12 trivalent vaccine: cross-season and cross-lineage protection with unchanged vaccine. J Infect Dis 210 (2014), 126–137.
44. 44 Skowronski, DM, Masaro, C, Kwindt, TL, et al. Estimating vaccine effectiveness against laboratory-confirmed influenza using a sentinel physician network: results from the 2005–2006 season of dual A and B vaccine mismatch in Canada. Vaccine 25 (2007), 2842–2851.
45. 45 Song, JY, Cheong, HJ, Heo, JY, et al. Effectiveness of the pandemic influenza A/H1N1 2009 monovalent vaccine in Korea. Vaccine 29 (2011), 1395–1398.
46. 46 Sullivan, SG, Komadina, N, Grant, K, Jelley, L, Papadakis, G, Kelly, H, Influenza vaccine effectiveness during the 2012 influenza season in Victoria, Australia: Influences of waning immunity and vaccine match. J Med Virol 86 (2014), 1017–1025.
47. 47 Treanor, JJ, Talbot, HK, Ohmit, SE, et al. Effectiveness of seasonal influenza vaccines in the United States during a season with circulation of all three vaccine strains. Clin Infect Dis 55 (2012), 951–959.
48. 48 Valenciano, M, Kissling, E, Cohen, JM, 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, 8, 2011, e1000388.
49. 49 Andrews, N, McMenamin, J, Durnall, H, et al. Effectiveness of trivalent seasonal influenza vaccine in preventing laboratory-confirmed influenza in primary care in the United Kingdom: 2012/13 end of season results. Euro Surveill 19 (2014), 5–13.
50. 50 Carville, KS, Grant, KA, Sullivan, SG, et al. Understanding influenza vaccine protection in the community: an assessment of the 2013 influenza season in Victoria, Australia. Vaccine 33 (2015), 341–345.
51. 51 Cost, AA, Hiser, MJ, Hu, Z, et al. Brief report: mid-season influenza vaccine effectiveness estimates for the 2013–2014 influenza season. MSMR 21 (2014), 15–17.
52. 52 Levy, A, Sullivan, SG, Tempone, SS, et al. Influenza vaccine effectiveness estimates for western Australia during a period of vaccine and virus strain stability, 2010 to 2012. Vaccine 32 (2014), 6312–6318.
53. 53 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 211 (2015), 1529–1540.
54. 54 Sullivan, SG, Chilver, MB, Higgins, G, Cheng, AC, Stocks, NP, Influenza vaccine effectiveness in Australia: results from the Australian Sentinel Practices Research Network. Med J Aust 201 (2014), 109–111.
55. 55 Turner, N, Pierse, N, Bissielo, A, et al. Effectiveness of seasonal trivalent inactivated influenza vaccine in preventing influenza hospitalisations and primary care visits in Auckland, New Zealand, in 2013. Euro Surveill, 19, 2014, 34.
56. 56 Turner, N, Pierse, N, Huang, QS, et al. Interim estimates of the effectiveness of seasonal trivalent inactivated influenza vaccine in preventing influenza hospitalisations and primary care visits in Auckland, New Zealand, in 2014. Euro Surveill, 19, 2014, 42.
57. 57 Yang, P, Thompson, MG, Ma, C, et al. Influenza vaccine effectiveness against medically-attended influenza illness during the 2012– 2013 season in Beijing, China. Vaccine 32 (2014), 5285–5289.
58. 58 Flannery, B, Clippard, J, Zimmerman, RK, et al. Early estimates of seasonal influenza vaccine effectiveness—United States, January 2015. MMWR Morb Mortal Wkly Rep 64 (2015), 10–15.
59. 59 Jimenez-Jorge, S, Pozo, F, Larrauri, A, et al. Interim influenza vaccine effectiveness: a good proxy for final estimates in Spain in the last four seasons 2010–2014. Vaccine 33 (2015), 3276–3280.
60. 60 McAnerney, JM, Treurnicht, F, Walaza, S, et al. Evaluation of influenza vaccine effectiveness and description of circulating strains in outpatient settings in South Africa, 2014. Influenza Other Respir Viruses 9 (2015), 209–215.
61. 61 Pebody, RG, Warburton, F, Ellis, J, et al. Low effectiveness of seasonal influenza vaccine in preventing laboratory-confirmed influenza in primary care in the United Kingdom: 2014/15 mid-season results. Euro Surveill, 20, 2015, 21025.
62. 62 Skowronski, DM, Chambers, C, Sabaiduc, S, et al. Interim estimates of 2014/15 vaccine effectiveness against influenza A(H3N2) from Canada's Sentinel Physician Surveillance Network, January 2015. Euro Surveill, 20, 2015, 4.
63. 63 Skowronski, DM, Chambers, C, Sabaiduc, S, et al. Integrated sentinel surveillance linking genetic, antigenic and epidemiologic monitoring of influenza vaccine-virus relatedness and effectiveness, 2013–14 season. J Infect Dis 212 (2015), 726–739.
64. 64 Jimenez-Jorge, S, de Mateo, S, Delgado-Sanz, C, et al. Effectiveness of influenza vaccine against laboratory-confirmed influenza, in the late 2011–2012 season in Spain, among population targeted for vaccination. BMC Infect Dis, 13, 2013, 441.
65. 65 Simonsen, L, Clarke, MJ, Williamson, GD, Stroup, DF, Arden, NH, Schonberger, LB, The impact of influenza epidemics on mortality: introducing a severity index. Am J Public Health 87 (1997), 1944–1950.
66. 66 Thompson, WW, Shay, DK, Weintraub, E, et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289 (2003), 179–186.
67. 67 Smith, DJ, Lapedes, AS, de Jong, JC, et al. Mapping the antigenic and genetic evolution of influenza virus. Science 305 (2004), 371–376.
68. 68 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 (in press).
69. 69 Darvishian, M, Bijlsma, MJ, Hak, E, van den Heuvel, ER, Effectiveness of seasonal influenza vaccine in community-dwelling elderly people: a meta-analysis of test-negative design case-control studies. Lancet Infect Dis 14 (2014), 1228–1239.
70. 70 Stohr, K, Bucher, D, Colgate, T, Wood, J, Influenza virus surveillance, vaccine strain selection, and manufacture. Methods Mol Biol 865 (2012), 147–162.
71. 71 Xu, X, Kilbourne, ED, Hall, HE, Cox, NJ, Nonimmunoselected intrastrain genetic variation detected in pairs of high-yielding influenza A (H3N2) vaccine and parental viruses. J Infect Dis 170 (1994), 1432–1438.
72. 72 McLean, HQ, Thompson, MG, Sundaram, ME, et al. Impact of repeated vaccination on vaccine effectiveness against influenza A(H3N2) and B during 8 seasons. Clin Infect Dis 59 (2014), 1375–1385.
73. 73 Sullivan, SG, Kelly, H, Stratified estimates of influenza vaccine effectiveness by prior vaccination: caution required. Clin Infect Dis 57 (2013), 474–476.
74. 74 Sullivan, SG, Feng, S, Cowling, BJ, Potential of the test-negative design for measuring influenza vaccine effectiveness: a systematic review. Expert Rev Vaccines 13 (2014), 1571–1591.
75. 75 WHO. Field guide for the evaluation of influenza vaccine effectiveness. http://www.who.int/immunization/research/development/VE_FieldGuide.pdf?ua=1, August, 2015 (accessed March 25, 2016).
76. 76 European Medicines Agency. Guideline on influenza vaccines. http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2014/07/WC500170300.pdf, July 25, 2014 (accessed March 25, 2016).