Comparative immunogenicity and safety of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine and HPV-6/11/16/18 vaccine administered according to 2- and 3-dose schedules in girls aged 9–14 years: Results to month 12 from a randomized trial

References

• Einstein MH, Baron M, Levin MJ, Chatterjee A, Edwards RP, Zepp F, Carletti I, Dessy FJ, Trofa AF, Schuind A, et al. 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
   PubMed Web of Science ®Google Scholar
• de Sanjosé S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR, et al. 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
   PubMed Web of Science ®Google Scholar
• Li N, Franceschi S, Howell-Jones R, Snijders PJ, Clifford GM. Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: Variation by geographical region, histological type and year of publication. Int J Cancer 2011; 128:927-35; PMID:20473886; http://dx.doi.org/10.1002/ijc.25396
   PubMed Web of Science ®Google Scholar
• Bruni L, Barrionuevo-Rosas L, Serrano B, Brotons M, Cosano R, Muñoz J, Bosch FX, de Sanjosé S. ICO information centre on HPV and cancer (HPV Information Centre). Human papillomavirus and related diseases in World. Summary Report 2014-08-22. Available from: http://www.hpvcentre.net/statistics/reports/XWX.pdf. Accessed 7 April 2015.
   Google Scholar
• Pedersen C, Petaja T, Strauss G, Rumke HC, Poder A, Richardus JH, Spiessens B, Descamps D, Hardt K, Lehtinen M, Dubin G. Immunization of early adolescent females with human papillomavirus type 16 and 18 L1 virus-like particle vaccine containing AS04 adjuvant. J Adolesc Health 2007; 40:564-71; PMID:17531764; http://dx.doi.org/10.1016/j.jadohealth.2007.02.015
   PubMed Web of Science ®Google Scholar
• Block SL, Nolan T, Sattler C, Barr E, Giacoletti KE, Marchant CD, Castellsague X, Rusche SA, Lukac S, Bryan JT, et al. Comparison of the immunogenicity and reactogenicity of a prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in male and female adolescents and young adult women. Pediatrics 2006; 118:2135-45; PMID:17079588; http://dx.doi.org/10.1542/peds.2006-0461
   PubMed Web of Science ®Google Scholar
• Harper DM, Franco EL, Wheeler C, Ferris DG, Jenkins D, Schuind A, Zahaf T, Innis B, Naud P, De Carvalho NS, et al. 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
   PubMed Web of Science ®Google Scholar
• Harper DM, Franco EL, Wheeler CM, Moscicki AB, Romanowski B, Roteli-Martins CM, Jenkins D, Schuind A, Costa Clemens SA, Dubin G. 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
   PubMed Web of Science ®Google Scholar
• Paavonen J, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter D, Kitchener H, Castellsague X, Teixeira JC, Skinner SR, et al. 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
   PubMed Web of Science ®Google Scholar
• Lehtinen M, Paavonen J, Wheeler CM, Jaisamrarn U, Garland SM, Castellsague X, Skinner SR, Apter D, Naud P, Salmeron J, et al. 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
   PubMed Web of Science ®Google Scholar
• Wheeler CM, Castellsague X, Garland SM, Szarewski A, Paavonen J, Naud P, Salmeron J, Chow SN, Apter D, Kitchener H, et al. 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
   PubMed Web of Science ®Google Scholar
• FUTURE II Study Group. Prophylactic efficacy of a quadrivalent human papillomavirus (HPV) vaccine in women with virological evidence of HPV infection. J Infect Dis 2007; 196:1438-46; PMID:18008221; http://dx.doi.org/10.1086/522864
   PubMed Web of Science ®Google Scholar
• Ault KA, FUTURE II Study Group. Effect of prophylactic human papillomavirus L1 virus-like-particle vaccine on risk of cervical intraepithelial neoplasia grade 2, grade 3, and adenocarcinoma in situ: a combined analysis of four randomised clinical trials. Lancet 2007; 369:1861-8; PMID:17544766; http://dx.doi.org/10.1016/S0140-6736(07)60852-6
   PubMed Web of Science ®Google Scholar
• Romanowski B, Schwarz TF, Ferguson LM, Peters K, Dionne M, Schulze K, Ramjattan B, Hillemanns P, Catteau G, Dobbelaere K, et al. Immunogenicity and safety of the HPV-16/18 AS04-adjuvanted vaccine administered as a 2-dose schedule compared to the licensed 3-dose schedule: Results from a randomized study. Hum Vaccin 2011; 7:1374-86; PMID:22048171; http://dx.doi.org/10.4161/hv.7.12.18322
   PubMed Web of Science ®Google Scholar
• Puthanakit T, Huang L, Tang R, Schwarz T, Esposito S, Frenette L, McNeil S, Rheault P, Horn M, Klar M, et al. Non-inferiority of HPV-16/18 AS04-adjuvanted vaccine administered as 2-dose schedules in girls (9-14 years) versus 3 doses in women (15-25 years): a randomised trial. Abstract presented at ESPID 2014. May 6-10, 2014. Dublin, Ireland. Available at: http://cmoffice.kenes.com/cddemo/data/HtmlApp/main.html#. Accessed 7 April 2015
   Google Scholar
• Romanowski B, Schwarz TF, Ferguson LM, Ferguson M, Peters K, Dionne M, Schulze K, Ramjattan B, Hillemanns P, Behre U, et al. Immune response to the HPV-16/18 AS04-adjuvanted vaccine administered as a 2-dose or 3-dose schedule up to 4 years after vaccination: Results from a randomized study. Hum Vaccin Immunother 2014; 10:1155-65; PMID:24576907; http://dx.doi.org/10.4161/hv.28022
   PubMed Web of Science ®Google Scholar
• Dobson SR, McNeil S, Dionne M, Dawar M, Ogilvie G, Krajden M, Sauvageau C, Scheifele DW, Kollmann TR, Halperin SA, et al. Immunogenicity of 2 doses of HPV vaccine in younger adolescents vs 3 doses in young women: a randomized clinical trial. JAMA 2013; 309:1793-802; PMID:23632723; http://dx.doi.org/10.1001/jama.2013.1625
   PubMed Web of Science ®Google Scholar
• European Medicines Agency. European public assessment report. Cervarix: human papillomavirus vaccine [types 16, 18] (recombinant, adjuvanted, adsorbed). EMEA/H/C/000721. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/EPAR_-_Summary_for_the_public/human/000721/WC500024634.pdf. Ac-cessed 7 April 2015.
   Google Scholar
• European Medicines Agency. European public assessment report. Gardasil: human papillomavirus vaccine [types 6, 11, 16, 18] (recombinant, adsorbed). EMEA/H/C/000703. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/EPAR_-_Summary_for_the_public/human/000703/WC500021146.pdf. Accessed 7 April 2015.
   Google Scholar
• Paavonen J, Jenkins D, Bosch FX, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter DL, Kitchener HC, Castellsagué X, et al. 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
   PubMed Web of Science ®Google Scholar
• Harper DM, Verdenius I, Ratnaraj F, Arey AM, Rosemergey B, Malnar GJ, Wall J. Quantifying clinical HPV4 dose inefficiencies in a safety net population. PLoS One 2013; 8:e77961; PMID:24223131; http://dx.doi.org/10.1371/journal.pone.0077961
   PubMedGoogle Scholar
• Markowitz LE, Tsu V, Deeks SL, Cubie H, Wang SA, Vicari AS, Brotherton JM. Human papillomavirus vaccine introduction-the first five years. Vaccine 2012; 30 Suppl 5:F139-48; PMID:23199957; http://dx.doi.org/10.1016/j.vaccine.2012.05.039
   PubMed Web of Science ®Google Scholar
• Hopkins TG, Wood N. Female human papillomavirus (HPV) vaccination: global uptake and the impact of attitudes. Vaccine 2013; 31:1673-9; PMID:23375978; http://dx.doi.org/10.1016/j.vaccine.2013.01.028
   PubMed Web of Science ®Google Scholar
• Harper DM, Verdenius I, Harris GD, Barnett AL, Rosemergey BE, Arey AM, Wall J, Malnar GJ. The influence of free quadrivalent human papillomavirus vaccine (HPV4) on the timely completion of the three dose series. Prev Med 2014; 61:20-5; PMID:24440159; http://dx.doi.org/10.1016/j.ypmed.2014.01.007
   PubMed Web of Science ®Google Scholar
• Einstein MH, Takacs P, Chatterjee A, Sperling RS, Chakhtoura N, Blatter MM, Lalezari J, David MP, Lin L, Struyf F, et al. Comparison of long-term immunogenicity and safety of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine and HPV-6/11/16/18 vaccine in healthy women aged 18-45 years: End-of-study analysis of a Phase III randomized trial. Hum Vaccin Immunother 2014;10:3435-45; PMID:25483701; http://dx.doi.org/10.4161/hv.36121
   PubMed Web of Science ®Google Scholar
• Draper E, Bissett SL, Howell-Jones R, Waight P, Soldan K, Jit M, Andrews N, Miller E, Beddows S. A randomized, observer-blinded immunogenicity trial of Cervarix® and Gardasil® human papillomavirus vaccines in 12-15 year old girls. PLoS One 2013; 8:e61825; PMID:23650505; http://dx.doi.org/10.1371/journal.pone.0061825
   PubMed Web of Science ®Google Scholar
• Toft L, Storgaard M, Muller M, Sehr P, Bonde J, Tolstrup M, Østergaard L, Søgaard OS. Comparison of the immunogenicity and reactogenicity of Cervarix and Gardasil human papillomavirus vaccines in HIV-infected adults: a randomized, double-blind clinical trial. J Infect Dis 2014; 209:1165-73; PMID:24273179; http://dx.doi.org/10.1093/infdis/jit657
   PubMed Web of Science ®Google Scholar
• Barzon L, Squarzon L, Masiero S, Pacenti M, Marcati G, Mantelli B, Gabrielli L, Lazzarotto T, Caputo A, Palu G. Neutralizing and cross-neutralizing antibody titres induced by bivalent and quadrivalent human papillomavirus vaccines in the target population of organized vaccination programmes. Vaccine 2014; 32:5357-62; PMID:25045814; http://dx.doi.org/10.1016/j.vaccine.2014.07.014
   PubMed Web of Science ®Google Scholar
• Castellsagué X, Naud P, Chow SN, Wheeler CM, Germar MJ, Lehtinen M, Paavonen J, Jaisamrarn U, Garland SM, Salmeron J, et al. Risk of newly detected infections and cervical abnormalities in women seropositive for naturally acquired human papillomavirus type 16/18 antibodies: analysis of the control arm of PATRICIA. J Infect Dis 2014; 210:517-34; PMID:24610876; http://dx.doi.org/10.1093/infdis/jiu139
   PubMed Web of Science ®Google Scholar
• Safaeian M, Porras C, Schiffman M, Rodriguez AC, Wacholder S, Gonzalez P, Quint W, van Doorn LJ, Sherman ME, Xhenseval V, et al. Epidemiological study of anti-HPV16/18 seropositivity and subsequent risk of HPV16 and −18 infections. J Natl Cancer Inst 2010; 102:1653-62; PMID:20944077; http://dx.doi.org/10.1093/jnci/djq384
   PubMedGoogle Scholar
• Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 2002; 298:2199-202; PMID:12481138; http://dx.doi.org/10.1126/science.1076071
   PubMed Web of Science ®Google Scholar
• Crotty S, Felgner P, Davies H, Glidewell J, Villarreal L, Ahmed R. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J Immunol 2003; 171:4969-73; PMID:14607890; http://dx.doi.org/10.4049/jimmunol.171.10.4969
   PubMed Web of Science ®Google Scholar
• Traggiai E, Puzone R, Lanzavecchia A. Antigen dependent and independent mechanisms that sustain serum antibody levels. Vaccine 2003; 21 Suppl 2:S35-7; PMID:12763680; http://dx.doi.org/10.1016/S0264-410X(03)00198-1
   PubMedGoogle Scholar
• Angelo MG, David MP, 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 2014; 23:466-79; PMID:24644063; http://dx.doi.org/10.1002/pds.3554
   PubMed Web of Science ®Google Scholar
• Angelo MG, 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 2014; 23:456-65; PMID:24644078; http://dx.doi.org/10.1002/pds.3593
   PubMed Web of Science ®Google Scholar
• Block SL, Brown DR, Chatterjee A, Gold MA, Sings HL, Meibohm A, Dana A, Haupt RM, Barr E, Tamms GM, et al. Clinical trial and post-licensure safety profile of a prophylactic human papillomavirus (types 6, 11, 16, and 18) l1 virus-like particle vaccine. Pediatr Infect Dis J 2010; 29:95-101; PMID:19952863; http://dx.doi.org/10.1097/INF.0b013e3181b77906
   PubMed Web of Science ®Google Scholar
• Garçon N, Chomez P, Van Mechelen M. GlaxoSmithKline Adjuvant Systems in vaccines: concepts, achievements and perspectives. Expert Rev Vaccines 2007; 6:723-39; PMID:17931153; http://dx.doi.org/10.1586/14760584.6.5.723
   PubMed Web of Science ®Google Scholar
• Garçon N, Morel S, Didierlaurent A, Descamps D, Wettendorff M, Van Mechelen M. Development of an AS04-adjuvanted HPV vaccine with the adjuvant system approach. BioDrugs 2011; 25:217-26; PMID:21815697; http://dx.doi.org/10.2165/11591760-000000000-00000
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Caulfield MJ, Shi L, Wang S, Wang B, Tobery TW, Mach H, Ahl PL, Cannon JL, Cook JC, Heinrichs JH, et al. Effect of alternative aluminum adjuvants on the absorption and immunogenicity of HPV16 L1 VLPs in mice. Hum Vaccin 2007; 3:139-45; PMID:17581283; http://dx.doi.org/10.4161/hv.3.4.4309
   PubMed Web of Science ®Google Scholar
• Dessy FJ, Giannini SL, Bougelet CA, Kemp TJ, David MP, 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
   PubMed Web of Science ®Google Scholar
• Robbins HA, Kemp TJ, Porras C, Rodriguez AC, Schiffman M, Wacholder S, Gonzalez P, Schiller J, Lowy D, Poncelet S, et al. Comparison of antibody responses to human papillomavirus vaccination as measured by three assays. Front Oncol 2014; 3:328; PMID:24455487; http://dx.doi.org/10.3389/fonc.2013.00328
   PubMedGoogle Scholar
• Pastrana DV, Buck CB, Pang YY, Thompson CD, Castle PE, FitzGerald PC, Kruger KS, 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
   PubMed Web of Science ®Google Scholar
• Crotty S, Aubert RD, Glidewell J, Ahmed R. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J Immunol Methods 2004; 286:111-22; PMID:15087226; http://dx.doi.org/10.1016/j.jim.2003.12.015
   PubMed Web of Science ®Google Scholar
• Einstein MH, Baron M, Levin MJ, Chatterjee A, Fox B, Scholar S, Rosen J, Chakhtoura N, Meric D, Dessy FJ, et al. Comparative immunogenicity and safety of human papillomavirus (HPV)-16/18 vaccine and HPV-6/11/16/18 vaccine: Follow-up from Months 12-24 in a Phase III randomized study of healthy women aged 18-45 years. Hum Vaccin 2011; 7:1343-58; PMID:22048173; http://dx.doi.org/10.4161/hv.7.12.18281
   PubMed Web of Science ®Google Scholar
• Moris P, van der Most R, Leroux-Roels I, Clement F, Drame M, Hanon E, Leroux-Roels GG, Van Mechelen M. H5N1 influenza vaccine formulated with AS03 A induces strong cross-reactive and polyfunctional CD4 T-cell responses. J Clin Immunol 2011; 31:443-54; PMID:21174144; http://dx.doi.org/10.1007/s10875-010-9490-6
   PubMed Web of Science ®Google Scholar
• Horton H, Thomas EP, Stucky JA, Frank I, Moodie Z, Huang Y, Chiu YL, McElrath MJ, De Rosa SC. Optimization and validation of an 8-color intracellular cytokine staining (ICS) assay to quantify antigen-specific T cells induced by vaccination. J Immunol Methods 2007; 323:39-54; PMID:17451739; http://dx.doi.org/10.1016/j.jim.2007.03.002
   PubMed Web of Science ®Google Scholar
• Chattopadhyay PK, Yu J, Roederer M. Live-cell assay to detect antigen-specific CD4+ T-cell responses by CD154 expression. Nat Protoc 2006; 1:1-6; PMID:17406204; http://dx.doi.org/10.1038/nprot.2006.1
   PubMed Web of Science ®Google Scholar
• Frentsch M, Arbach O, Kirchhoff D, Moewes B, Worm M, Rothe M, Scheffold A, Thiel A. Direct access to CD4+ T cells specific for defined antigens according to CD154 expression. Nat Med 2005; 11:1118-24; PMID:16186818; http://dx.doi.org/10.1038/nm1292
   PubMed Web of Science ®Google Scholar
• International Conference on Harmonisation of Technical Requirements for Registration of Pharmaceuticals for Human Use. ICH Harmonised Tripartite Guideline. Statistical Principles for Clinical Trials (E9). 5 February 1998. Available from: http://www.ich.org/fileadmin/Public_Web_Site/ICH_Products/Guidelines/Efficacy/E9/Step4/E9_Guideline.pdf. Accessed 7 April 2015.
   Google Scholar