Sustained efficacy, immunogenicity, and safety of the HPV-16/18 AS04-adjuvanted vaccine: Final analysis of a long-term follow-up study up to 9.4 years post-vaccination

Human Vaccines and Immunotherapeutics

Volumn 10, Issue 8, 2014, Pages 2147-2162

  Naud, Paulo S ^a   Roteli Martins, Cecilia M ^b   De Carvalho, Newton S ^c   Teixeira, Julio C ^d   De Borba, Paola C ^e   Sanchez, Nervo ^f   Zahaf, Toufik ^g   Catteau, Gregory ^g   Geeraerts, Brecht ^g   Descamps, Dominique ^g  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b HOSPITAL MATERNIDADE LEONOR MENDES DE BARROS   (Brazil)

^c FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^d UNIVERSITY OF CAMPINAS   (Brazil)

^e Institute of Cancer   (Brazil)

^f Independent Researchers Cia Ltda   (Brazil)

^g GSK   (Belgium)

Author keywords

Cervical cancer; Efficacy; HPV 16 18 AS04 adjuvanted vaccine; Human papillomavirus (HPV); Immunogenicity; Long term protection; Pre cancer; Safety

Indexed keywords

WART VIRUS VACCINE; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY; VIRUS DNA;

ADOLESCENT; ADULT; ANTIBODY RESPONSE; ARTICLE; BRAZIL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; DRUG SAFETY; FEMALE; FOLLOW UP; HISTOPATHOLOGY; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOGENICITY; LONG TERM CARE; MAJOR CLINICAL STUDY; MULTICENTER STUDY; PAPILLOMAVIRUS INFECTION; RANDOMIZED CONTROLLED TRIAL; UTERINE CERVIX CARCINOMA IN SITU; YOUNG ADULT; BLOOD; CLINICAL TRIAL; CYTOCHEMISTRY; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; PAPILLOMAVIRUS INFECTIONS; SERODIAGNOSIS; TREATMENT OUTCOME; UTERINE CERVICAL NEOPLASMS; VAGINA SMEAR;

ADOLESCENT; ADULT; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BRAZIL; DNA, VIRAL; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FOLLOW-UP STUDIES; HISTOCYTOCHEMISTRY; HUMAN PAPILLOMAVIRUS 16; HUMAN PAPILLOMAVIRUS 18; HUMANS; NEUTRALIZATION TESTS; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; TREATMENT OUTCOME; UTERINE CERVICAL NEOPLASMS; VAGINAL SMEARS; YOUNG ADULT;

EID: 84908371999     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.29532     Document Type: Article

References (34)

1. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJF, Peto J, Meijer CJLM, Muñoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999; 189:12-9; PMID:10451482; http://dx.doi.org/10.1002/(SICI)1096-9896(199909)189:1〈12::AIDPATH431〉3.0.CO;2-F
2. Bosch FX, Lorincz A, Muñoz N, Meijer CJLM, Shah KV. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002; 55:244-65; PMID:11919208; http://dx.doi.org/10.1136/jcp.55.4.244
3. Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, Snijders PJ, Meijer CJLM; International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003; 348:518-27; PMID:12571259; http://dx.doi.org/10.1056/NEJMoa021641
4. Schiffman M, Clifford G, Buonaguro FM. Classification of weakly carcinogenic human papillomavirus types: addressing the limits of epidemiology at the borderline. Infect Agent Cancer 2009; 4:8; PMID:19486508; http://dx.doi.org/10.1186/1750-9378-4-8
5. de Sanjose S, Quint WGV, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin H-R, et al.; Retrospective International Survey and HPV Time Trends Study Group. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol 2010; 11:1048-56; PMID:20952254; http://dx.doi.org/10.1016/S1470-2045(10)70230-8
6. Wheeler CM, Castellsagué X, Garland SM, Szarewski A, Paavonen J, Naud P, Salmerón J, Chow S-N, Apter D, Kitchener H, et al.; HPV PATRICIA Study Group. Cross-protective efficacy of HPV-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by non-vaccine oncogenic HPV types: 4-year end-of-study analysis of the randomised, double-blind PATRICIA trial. Lancet Oncol 2012; 13:100-10; PMID:22075170; http://dx.doi.org/10.1016/S1470-2045(11)70287-X
7. Castellsagué X, Schneider A, Kaufmann AM, Bosch FX. HPV vaccination against cervical cancer in women above 25 years of age: key considerations and current perspectives. Gynecol Oncol 2009; 115(Suppl):S15-23; PMID:19819540; http://dx.doi.org/10.1016/j.ygyno.2009.09.021
8. Roteli-Martins CM, Naud P, De Borba P, Teixeira JC, De Carvalho NS, Zahaf T, Sanchez N, Geeraerts B, Descamps D. Sustained immunogenicity and efficacy of the HPV-16/18 AS04-adjuvanted vaccine: up to 8.4 years of follow-up. Hum Vaccin Immunother 2012; 8:390-7; PMID:22327492; http://dx.doi.org/10.4161/hv.18865
9. Rowhani-Rahbar A, Alvarez FB, Bryan JT, Hughes JP, Hawes SE, Weiss NS, Koutsky LA. Evidence of immune memory 8.5 years following administration of a prophylactic human papillomavirus type 16 vaccine. J Clin Virol 2012; 53:239-43; PMID:22209292; http://dx.doi.org/10.1016/j.jcv.2011.12.009
10. Giannini SL, Hanon E, Moris P, Van Mechelen M, Morel S, Dessy F, Fourneau MA, Colau B, Suzich J, Losonksy G, et al. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine 2006; 24:5937-49; PMID:16828940; http://dx.doi.org/10.1016/j.vaccine.2006.06.005
11. De Carvalho N, Teixeira J, Roteli-Martins CM, Naud P, De Borba P, Zahaf T, Sanchez N, Schuind A. Sustained efficacy and immunogenicity of the HPV-16/18 AS04-adjuvanted vaccine up to 7.3 years in young adult women. Vaccine 2010; 28:6247-55; PMID:20643092; http://dx.doi.org/10.1016/j.vaccine.2010.07.007
12. Moscicki AB, Wheeler CM, Romanowski B, Hedrick J, Gall S, Ferris D, Poncelet S, Zahaf T, Moris P, Geeraerts B, et al. Immune responses elicited by a fourth dose of the HPV-16/18 AS04-adjuvanted vaccine in previously vaccinated adult women. Vaccine 2012; 31:234-41; PMID:23063422; http://dx.doi.org/10.1016/j.vaccine.2012.09.037
13. Petäjä T, Pedersen C, Poder A, Strauss G, Catteau G, Thomas F, Lehtinen M, Descamps D. Long-term persistence of systemic and mucosal immune response to HPV-16/18 AS04-adjuvanted vaccine in preteen/adolescent girls and young women. Int J Cancer 2011; 129:2147-57; PMID:21190190; http://dx.doi.org/10.1002/ijc.25887
14. Schwarz TF, Spaczynski M, Schneider A, Wysocki J, Galaj A, Schulze K, Poncelet SM, Catteau G, Thomas F, Descamps D. Persistence of immune response to HPV-16/18 AS04-adjuvanted cervical cancer vaccine in women aged 15-55 years. Hum Vaccin 2011; 7:958-65; PMID:21892005; http://dx.doi.org/10.4161/hv.7.9.15999
15. Schwarz TF, Huang L-M, Medina DMR, Valencia A, Lin T-Y, Behre U, Catteau G, Thomas F, Descamps Dl. Four-Year follow-up of the immunogenicity and safety of the HPV-16/18 AS04-Adjuvanted vaccine when administered to adolescent girls aged 10-14 years. J Adol Hlth 2012; 50:187-94; http://dx.doi.org/10.1016/j.jadohealth.2011.11.004
16. Paavonen J, Jenkins D, Bosch FX, Naud P, Salmerón J, Wheeler CM, Chow S-N, Apter DL, Kitchener HC, Castellsague X, et al.; HPV PATRICIA study group. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial. Lancet 2007; 369:2161-70; PMID:17602732; http://dx.doi.org/10.1016/S0140-6736(07)60946-5
17. Paavonen J, Naud P, Salmerón J, Wheeler CM, Chow S-N, Apter D, Kitchener H, Castellsague X, Teixeira JC, Skinner SR, et al.; HPV PATRICIA Study Group. Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 2009; 374:301-14; PMID:19586656; http://dx.doi.org/10.1016/S0140-6736(09)61248-4
18. Lehtinen M, Paavonen J, Wheeler CM, Jaisamrarn U, Garland SM, Castellsagué X, Skinner SR, Apter D, Naud P, Salmerón J, et al.; HPV PATRICIA Study Group. Overall efficacy of HPV-16/18 AS04-adjuvanted vaccine against grade 3 or greater cervical intraepithelial neoplasia: 4-year end-of-study analysis of the randomised, double-blind PATRICIA trial. Lancet Oncol 2012; 13:89-99; PMID:22075171; http://dx.doi.org/10.1016/S1470-2045(11)70286-8
19. Verstraeten T, Descamps D, David M-P, Zahaf T, Hardt K, Izurieta P, Dubin G, Breuer T. Analysis of adverse events of potential autoimmune aetiology in a large integrated safety database of AS04 adjuvanted vaccines. Vaccine 2008; 26:6630-8; PMID:18845199; http://dx.doi.org/10.1016/j.vaccine.2008.09.049
20. Descamps D, Hardt K, Spiessens B, Izurieta P, Verstraeten T, Breuer T, Dubin G. Safety of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine for cervical cancer prevention: a pooled analysis of 11 clinical trials. Hum Vaccin 2009; 5:332-40; PMID:19221517; http://dx.doi.org/10.4161/hv.5.5.7211
21. Harper DM, Franco EL, Wheeler C, Ferris DG, Jenkins D, Schuind A, Zahaf T, Innis B, Naud P, De Carvalho NS, et al.; GlaxoSmithKline HPV Vaccine Study Group. Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet 2004; 364:1757-65; PMID:15541448; http://dx.doi.org/10.1016/S0140-6736(04)17398-4
22. Harper DM, Franco EL, Wheeler CM, Moscicki A-B, Romanowski B, Roteli-Martins CM, Jenkins D, Schuind A, Costa Clemens SA, Dubin G; HPV Vaccine Study group. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet 2006; 367:1247-55; PMID:16631880; http://dx.doi.org/10.1016/S0140-6736(06)68439-0
23. The GlaxoSmithKline Vaccine HPV-007 Study Group. Sustained efficacy and immunogenicity of the HPV-16/18 AS04-adjuvanted vaccine: analysis of a randomised placebo-controlled trial up to 6.4 years. Lancet 2009; 374:1975-85; PMID:19962185; http://dx.doi.org/10.1016/S0140-6736(09)61567-1
24. Einstein MH, Baron M, Levin MJ, Chatterjee A, Edwards RP, Zepp F, Carletti I, Dessy FJ, Trofa AF, Schuind A, et al.; HPV-010 Study Group. Comparison of the immunogenicity and safety of Cervarix and Gardasil human papillomavirus (HPV) cervical cancer vaccines in healthy women aged 18-45 years. Hum Vaccin 2009; 5:705-19; PMID:19684472; http://dx.doi.org/10.4161/hv.5.10.9518
25. Dessy FJ, Giannini SL, Bougelet CA, Kemp TJ, David M-PM, Poncelet SM, Pinto LA, Wettendorff MA. Correlation between direct ELISA, single epitope-based inhibition ELISA and pseudovirion-based neutralization assay for measuring anti-HPV-16 and anti-HPV-18 antibody response after vaccination with the AS04-adjuvanted HPV-16/18 cervical cancer vaccine. Hum Vaccin 2008; 4:425-34; PMID:18948732; http://dx.doi.org/10.4161/hv.4.6.6912
26. David MP, Van Herck K, Hardt K, Tibaldi F, Dubin G, Descamps D, Van Damme P. Long-term persistence of anti-HPV-16 and -18 antibodies induced by vaccination with the AS04-adjuvanted cervical cancer vaccine: modeling of sustained antibody responses. Gynecol Oncol 2009; 115(Suppl):S1-6; PMID:19217149; http://dx.doi.org/10.1016/j.ygyno.2009.01.011
27. Fraser C, Tomassini JE, Xi L, Golm G, Watson M, Giuliano AR, Barr E, Ault KA. Modeling the long-term antibody response of a human papillomavirus (HPV) virus-like particle (VLP) type 16 prophylactic vaccine. Vaccine 2007; 25:4324-33; PMID:17445955; http://dx.doi.org/10.1016/j.vaccine.2007.02.069
28. Herrero R, Wacholder S, Rodríguez AC, Solomon D, González P, Kreimer AR, Porras C, Schussler J, Jiménez S, Sherman ME, et al.; Costa Rica Vaccine Trial Group. Prevention of persistent human papillomavirus infection by an HPV16/18 vaccine: a community-based randomized clinical trial in Guanacaste, Costa Rica. Cancer Discov 2011; 1:408-19; PMID:22586631; http://dx.doi.org/10.1158/2159-8290.CD-11-0131
29. Kreimer AR, Rodriguez AC, Hildesheim A, Herrero R, Porras C, Schiffman M, González P, Solomon D, Jiménez S, Schiller JT, et al.; CVT Vaccine Group. Proof-of-principle evaluation of the efficacy of fewer than three doses of a bivalent HPV16/18 vaccine. J Natl Cancer Inst 2011a; 103:1444-51; PMID:21908768; http://dx.doi.org/10.1093/jnci/djr319
30. Angelo M-G, David M-P, Zima J, Baril L, Dubin G, Arellano F, Struyf F. Pooled analysis of large and long-term safety data from the human papillomavirus-16/18-AS04-adjuvanted vaccine clinical trial programme. Pharmacoepidemiol Drug Saf 2014a; 23:466-79; PMID:24644063; http://dx.doi.org/10.1002/pds.3554
31. Angelo M-G, Zima J, Tavares Da Silva F, Baril L, Arellano F. Post-licensure safety surveillance for human papillomavirus-16/18-AS04-adjuvanted vaccine: more than 4 years of experience. Pharmacoepidemiol Drug Saf 2014b; 23:456-65; PMID:24644078; http://dx.doi.org/10.1002/pds.3593
32. Wacholder S, Chen BE, Wilcox A, Macones G, Gonzalez P, Befano B, Hildesheim A, Rodríguez AC, Solomon D, Herrero R, et al.; CVT group. Risk of miscarriage with bivalent vaccine against human papillomavirus (HPV) types 16 and 18: pooled analysis of two randomised controlled trials. BMJ 2010; 340:c712; PMID:20197322; http://dx.doi.org/10.1136/bmj.c712
33. van Doorn LJ, Molijn A, Kleter B, Quint W, Colau B. Highly effective detection of human papillomavirus 16 and 18 DNA by a testing algorithm combining broad-spectrum and type-specific PCR. J Clin Microbiol 2006; 44:3292-8; PMID:16954263; http://dx.doi.org/10.1128/JCM.00539-06
34. Pastrana DV, Buck CB, Pang Y-YS, Thompson CD, Castle PE, FitzGerald PC, Krüger Kjaer S, Lowy DR, Schiller JT. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 2004; 321:205-16; PMID:15051381; http://dx.doi.org/10.1016/j.virol.2003.12.027