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. 2018 May 9;5(5):CD009069.
doi: 10.1002/14651858.CD009069.pub3.

Prophylactic vaccination against human papillomaviruses to prevent cervical cancer and its precursors

Marc Arbyn  1 , Lan Xu, Cindy Simoens, Pierre Pl Martin-Hirsch
Affiliations

Prophylactic vaccination against human papillomaviruses to prevent cervical cancer and its precursors

Marc Arbyn et al. Cochrane Database Syst Rev. .

Abstract

Background: Persistent infection with high-risk human papillomaviruses (hrHPV) types is causally linked with the development of cervical precancer and cancer. HPV types 16 and 18 cause approximately 70% of cervical cancers worldwide.

Objectives: To evaluate the harms and protection of prophylactic human papillomaviruses (HPV) vaccines against cervical precancer and HPV16/18 infection in adolescent girls and women.

Search methods: We searched MEDLINE, Cochrane Central Register of Controlled Trials (CENTRAL) and Embase (June 2017) for reports on effects from trials. We searched trial registries and company results' registers to identify unpublished data for mortality and serious adverse events.

Selection criteria: Randomised controlled trials comparing efficacy and safety in females offered HPV vaccines with placebo (vaccine adjuvants or another control vaccine).

Data collection and analysis: We used Cochrane methodology and GRADE to rate the certainty of evidence for protection against cervical precancer (cervical intraepithelial neoplasia grade 2 and above [CIN2+], CIN grade 3 and above [CIN3+], and adenocarcinoma-in-situ [AIS]), and for harms. We distinguished between the effects of vaccines by participants' baseline HPV DNA status. The outcomes were precancer associated with vaccine HPV types and precancer irrespective of HPV type. Results are presented as risks in control and vaccination groups and risk ratios (RR) with 95% confidence intervals in brackets.

Main results: We included 26 trials (73,428 participants). Ten trials, with follow-up of 1.3 to 8 years, addressed protection against CIN/AIS. Vaccine safety was evaluated over a period of 6 months to 7 years in 23 studies. Studies were not large enough or of sufficient duration to evaluate cervical cancer outcomes. All but one of the trials was funded by the vaccine manufacturers. We judged most included trials to be at low risk of bias. Studies involved monovalent (N = 1), bivalent (N = 18), and quadrivalent vaccines (N = 7). Most women were under 26 years of age. Three trials recruited women aged 25 and over. We summarize the effects of vaccines in participants who had at least one immunisation.Efficacy endpoints by initial HPV DNA statushrHPV negativeHPV vaccines reduce CIN2+, CIN3+, AIS associated with HPV16/18 compared with placebo in adolescent girls and women aged 15 to 26. There is high-certainty evidence that vaccines lower CIN2+ from 164 to 2/10,000 (RR 0.01 (0 to 0.05)) and CIN3+ from 70 to 0/10,000 (RR 0.01 (0.00 to 0.10). There is moderate-certainty evidence that vaccines reduce the risk of AIS from 9 to 0/10,000 (RR 0.10 (0.01 to 0.82).HPV vaccines reduce the risk of any CIN2+ from 287 to 106/10,000 (RR 0.37 (0.25 to 0.55), high certainty) and probably reduce any AIS lesions from 10 to 0/10,000 (RR 0.1 (0.01 to 0.76), moderate certainty). The size of reduction in CIN3+ with vaccines differed between bivalent and quadrivalent vaccines (bivalent: RR 0.08 (0.03 to 0.23), high certainty; quadrivalent: RR 0.54 (0.36 to 0.82), moderate certainty). Data in older women were not available for this comparison.HPV16/18 negativeIn those aged 15 to 26 years, vaccines reduce CIN2+ associated with HPV16/18 from 113 to 6 /10,000 (RR 0.05 (0.03 to 0.10). In women 24 years or older the absolute and relative reduction in the risk of these lesions is smaller (from 45 to 14/10,000, (RR 0.30 (0.11 to 0.81), moderate certainty). HPV vaccines reduce the risk of CIN3+ and AIS associated with HPV16/18 in younger women (RR 0.05 (0.02 to 0.14), high certainty and RR 0.09 (0.01 to 0.72), moderate certainty, respectively). No trials in older women have measured these outcomes.Vaccines reduce any CIN2+ from 231 to 95/10,000, (RR 0.41 (0.32 to 0.52)) in younger women. No data are reported for more severe lesions.Regardless of HPV DNA statusIn younger women HPV vaccines reduce the risk of CIN2+ associated with HPV16/18 from 341 to 157/10,000 (RR 0.46 (0.37 to 0.57), high certainty). Similar reductions in risk were observed for CIN3+ associated with HPV16/18 (high certainty). The number of women with AIS associated with HPV16/18 is reduced from 14 to 5/10,000 with HPV vaccines (high certainty).HPV vaccines reduce any CIN2+ from 559 to 391/10,000 (RR 0.70 (0.58 to 0.85, high certainty) and any AIS from 17 to 5/10,000 (RR 0.32 (0.15 to 0.67), high certainty). The reduction in any CIN3+ differed by vaccine type (bivalent vaccine: RR 0.55 (0.43 to 0.71) and quadrivalent vaccine: RR 0.81 (0.69 to 0.96)).In women vaccinated at 24 to 45 years of age, there is moderate-certainty evidence that the risks of CIN2+ associated with HPV16/18 and any CIN2+ are similar between vaccinated and unvaccinated women (RR 0.74 (0.52 to 1.05) and RR 1.04 (0.83 to 1.30) respectively). No data are reported in this age group for CIN3+ or AIS.Adverse effectsThe risk of serious adverse events is similar between control and HPV vaccines in women of all ages (669 versus 656/10,000, RR 0.98 (0.92 to 1.05), high certainty). Mortality was 11/10,000 in control groups compared with 14/10,000 (9 to 22) with HPV vaccine (RR 1.29 [0.85 to 1.98]; low certainty). The number of deaths was low overall but there is a higher number of deaths in older women. No pattern in the cause or timing of death has been established.Pregnancy outcomesAmong those who became pregnant during the studies, we did not find an increased risk of miscarriage (1618 versus 1424/10,000, RR 0.88 (0.68 to 1.14), high certainty) or termination (931 versus 838/10,000 RR 0.90 (0.80 to 1.02), high certainty). The effects on congenital abnormalities and stillbirths are uncertain (RR 1.22 (0.88 to 1.69), moderate certainty and (RR 1.12 (0.68 to 1.83), moderate certainty, respectively).

Authors' conclusions: There is high-certainty evidence that HPV vaccines protect against cervical precancer in adolescent girls and young women aged 15 to 26. The effect is higher for lesions associated with HPV16/18 than for lesions irrespective of HPV type. The effect is greater in those who are negative for hrHPV or HPV16/18 DNA at enrolment than those unselected for HPV DNA status. There is moderate-certainty evidence that HPV vaccines reduce CIN2+ in older women who are HPV16/18 negative, but not when they are unselected by HPV DNA status.We did not find an increased risk of serious adverse effects. Although the number of deaths is low overall, there were more deaths among women older than 25 years who received the vaccine. The deaths reported in the studies have been judged not to be related to the vaccine. Increased risk of adverse pregnancy outcomes after HPV vaccination cannot be excluded, although the risk of miscarriage and termination are similar between trial arms. Long-term of follow-up is needed to monitor the impact on cervical cancer, occurrence of rare harms and pregnancy outcomes.

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Conflict of interest statement

MA: has received travel grants from MSD‐Sanofi‐Pasteur and GSK, (ceased in 2008). PM‐H: travel grants received from GSK and MSD‐Sanofi‐Pasteur (ceased in 2008). LX: no conflict of interest. CS received travel grant from GSK (2007).

Authors of this review were assessed by the Cochrance Funding Arbiter Committee after Cochrane received correspondence and feedback on the published protocol. Current authors were approved by this committee based on stringent Cochrane conflict of interest guidelines. A unrestricted grant was provided by Sanofi‐Pasteur‐MSD to the University of Ghent who co‐ordinated the SEHIB study (Surveillance of Effects of HPV Immunisation in Belgium). The grant was given in the framework of the EMA (European Medicine Agency) request to set up post‐marketing surveillance of HPV vaccination effects in non‐Nordic member states of the European Union. The Sciensano (employer of MA and LX, former name “Scientific Institute of Public Health”) collaborated with the University of Ghent to conduct the SEHIB study.

Figures

1
1
Flow diagram summarising the retrieval, inclusion and exclusion of relevant reports of randomised trials assessing the safety and effects of prophylactic HPV vaccines.
2
2
'Risk of bias' summary: review authors' judgements about each 'Risk of bias' item for each included study.
 V1 = Random sequence generation; V2 = Allocation concealment; V3 = Blinding participants & personnel; V4 = Blinding of outcome assessment; V5 = Incomplete outcomes; V6 = Selective reporting.
3
3
'Risk of bias' graph: review authors' judgements about each 'Risk of bias' item presented as percentages across all included studies.
4
4
'Risk of bias' summary: review authors' judgements about each 'Risk of bias' item for each included study.
5
5
Protection against CIN2+ irrespective of presence of HPV types in women, aged 15‐26 years, regardless of their HPV DNA status at baseline, who received at least one dose.
6
6
Summary of vaccine efficacy estimates, by age group, outcome and HPV DNA status at enrolment (for women who received at least one dose). [REFS BETWEEN SQUARE BRACKETS MUST BE ADAPTED][
7
7
Summary of vaccine efficacy estimates by age group, outcome and number of received doses (for women who were HPV16/18 DNA negative at enrolment). [REFS BETWEEN SQUARE BRACKETS MUST BE ADAPTED][
8
8
Modified Cates plot: Number of cases of CIN2+ associated with HPV16/18 occurring in women who were all hrHPV DNA negative at baseline. 16 out of 1000 non‐vaccinated women developed the lesion (left) whereas fewer than one (0.2) out 1000 vaccinated women developed the lesion (right). Relative risk= 0.01 (95% CI: 0.01 to 0.05).
9
9
Modified Cates plot: Number of cases of CIN2+ irrespective of HPV types occurring in women who were all hrHPV DNA negative at baseline. 28 out of 1000 non‐vaccinated women developed the lesion (left) whereas 11 out 1000 vaccinated women developed the lesion (right). Relative risk= 0.37 (95% CI: 0.25 to 0.55).
10
10
Sensitivity analysis of Analysis 7.6 on severe adverse effects restricting to data extracted from publications in peer‐reviewed journals.
11
11
Sensitivity analysis of Analysis 7.7 on deaths restricting to data extracted from publications in peer‐reviewed journals.
12
12
Protection against CIN2+ associated with HPV16/18 in women, aged 15‐26 years, who were HPV DNA 16/18 negative at baseline, by number of doses.
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    1. Harper DM, Franco EL, Wheeler C, Ferris DG, Jenkins D, Schuind A. 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(9447):1757‐65. - PubMed
    1. Harper DM, Franco EL, Wheeler CM, Moscicki AB, Romanowski B, Roteli‐Martins CM. 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(9518):1247‐55. - PubMed
    1. Naud PS, Roteli‐Martins CM, Carvalho NS, Teixeira JC, Borba PC, Sanchez N, et al. 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 & Immunotherapeutics 2014;10(8):2147‐62. - PMC - PubMed
    1. The GlaxoSmithKline Vaccine HPV‐007 Study Group. Sustained efficacy and immunogenicity of the human papillomavirus (HPV)‐16/18 ASO4‐adjuvanted vaccine: analysis of a randomised placebo‐controlled trial up to 6.4 years. Lancet 2009;374:1975‐85. - PubMed
Phase2 trial (ph2,4v) {published data only}
    1. Olsson SE, Kjaer SK, Sigurdsson K, Iversen OE. Evaluation of quadrivalent HPV 6/11/16/18 vaccine efficacy against cervical and anogenital disease in subjects with serological evidence of prior vaccine type HPV infection. Human Vaccines 2009;5(10):696‐704. - PubMed
    1. Villa LL, Ault KA, Giuliano AR, Costa RL, Petta CA, Andrade RP. Immunologic responses following administration of a vaccine targeting human papillomavirus Types 6, 11, 16, and 18. Vaccine 2006;24(27):5571‐83. - PubMed
    1. Villa LL, Costa RL, Petta CA, Andrade RP, Ault KA, Giuliano AR. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus‐like particle vaccine in young women: a randomised double‐blind placebo‐controlled multicentre phase II efficacy trial. Lancet Oncology 2005;6(5):271‐8. - PubMed
    1. Villa LL, Costa RL, Petta CA, Andrade RP, Paavonen J, Iversen OE. High sustained efficacy of a prophylactic quadrivalent human papillomavirus types 6/11/16/18 L1 virus‐like particle vaccine through 5 years of follow‐up. British Journal of Cancer 2006;95(11):1459‐66. - PMC - PubMed
VIVIANE trial (ph3,2v) {published data only}
    1. Skinner SR, Szarewski A, Romanowski B, Garland SM, Lazcano‐Ponce E, Salmeron J. Efficacy, safety, and immunogenicity of the human papillomavirus 16/18 AS04‐adjuvanted vaccine in women older than 25 years: 4‐year interim follow‐up of the phase 3, double‐blind, randomised controlled VIVIANE study. Lancet 2014;384(9961):2213‐27. - PubMed
    1. Wheeler CM, Skinner SR, Rosario‐Raymundo MR, Garland SM, Chatterjee A, Lazcano‐Ponce E, et al. Efficacy, safety, and immunogenicity of the human papillomavirus 16/18 AS04‐adjuvanted vaccine in women older than 25 years: 7‐year interim follow‐up of the phase 3, double‐blind, randomised controlled VIVIANE study. Lancet Infectious Diseases 2016;16(10):1154–68. - PubMed

References to studies excluded from this review

Angelo 2014 {published data only}
    1. Angelo MG, David MP, Zima J, Baril L, Dubin G, Arellano F, et al. Pooled analysis of large and long‐term safety data from the human papillomavirus‐16/18‐AS04‐adjuvanted vaccine clinical trial programme. Pharmacoepidemiology and Drug Safety 2014;23(1099‐557 (Electronic), 1053‐8569 (Linking), 5):466‐79. - PMC - PubMed
Arguedas 2010 {published data only}
    1. Arguedas A, Soley C, Loaiza C, Rincon G, Guevara S, Perez A, et al. Safety and immunogenicity of one dose of MenACWY‐CRM, an investigational quadrivalent meningococcal glycoconjugate vaccine, when administered to adolescents concomitantly or sequentially with Tdap and HPV vaccines. Vaccine 2010;28(1873‐2518 (Electronic), 0264‐410X (Linking), 18):3171‐9. - PubMed
Ault 2004 {published data only}
    1. Ault KA, Giuliano AR, Edwards RP, Tamms G, Kim LL, Smith JF. A phase I study to evaluate a human papillomavirus (HPV) type 18 L1 VLP vaccine. Vaccine 2004;22(23‐24):3004‐7. - PubMed
Ault 2007 {published data only}
    1. 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(9576):1861‐8. - PubMed
Basu 2013 {published data only}
    1. Basu P, Banerjee D, Singh P, Bhattacharya C, Biswas J. Efficacy and safety of human papillomavirus vaccine for primary prevention of cervical cancer: A review of evidence from phase III trials and national programs. South Asian Journal of Cancer 2013;2(4):187‐92. - PMC - PubMed
Beachler 2016 {published data only}
    1. Beachler DC, Kreimer AR, Schiffman M, Herrero R, Wacholder S, Rodriguez AC, et al. Multisite HPV16/18 vaccine efficacy against cervical, anal, and oral HPV infection. Journal of the National Cancer Institute 2016;108(1):djv302. - PMC - PubMed
Brown 2004 {published data only}
    1. Brown DR, Fife KH, Wheeler CM, Koutsky LA, Lupinacci LM, Railkar R. Early assessment of the efficacy of a human papillomavirus type 16 L1 virus‐like particle vaccine. Vaccine 2004;22(21‐22):2936‐42. - PubMed
Couto 2014 {published data only}
    1. Couto E, Saeterdal I, Juvet LK, Klemp M. HPV catch‐up vaccination of young women: a systematic review and meta‐analysis. BMC Public Health 2014;14(1471‐2458 (Electronic), 1471‐2458 (Linking)):867. - PMC - PubMed
D'Addario 2017 {published data only}
    1. D'Addario M, Redmond S, Scott P, Egli‐Gany D, Riveros‐Balta AX, Henao Restrepo AM, et al. Two‐dose schedules for human papillomavirus vaccine: Systematic review and meta‐analysis. Vaccine 2017;35(1873‐2518 (Electronic), 0264‐410X (Linking), 22):2892‐901. - PubMed
D'Souza 2013 {published data only}
    1. D'Souza C, Mort GS, Zyngier S, Robinson P, Schlotterlein M. Preventive innovation: an Australian case study on HPV vaccination. Health Marketing Quartely 2013;30(3):206‐20. - PubMed
Delere 2013 {published data only}
    1. Delere Y, Bohmer MM, Walter D, Wichmann O. HPV vaccination coverage among women aged 18‐20 years in Germany three years after recommendation of HPV vaccination for adolescent girls: results from a cross‐sectional survey. Human Vaccines & Immunotherapeutics 2013;9(8):1706‐11. - PMC - PubMed
Denny 2013 {published data only}
    1. Denny L, Hendricks B, Gordon C, Thomas F, Hezareh M, Dobbelaere K. Safety and immunogenicity of the HPV‐16/18 AS04‐adjuvanted vaccine in HIV‐positive women in South Africa: A partially‐blind randomised placebo‐controlled study. Vaccine 2013;31(48):5745‐53. - PubMed
Descamps 2009 {published data only}
    1. Descamps D, Hardt K, Spiessens B, Izurieta P, Verstraeten T, Breuer T. Safety of human papillomavirus (HPV)‐16/18 AS04‐adjuvanted vaccine for cervical cancer prevention: a pooled analysis of 11 clinical trials. Human Vaccines & Immunotherapeutics 2009;5(5):332‐40. - PubMed
De Vincenzo 2014 {published data only}
    1. Vincenzo R, Conte C, Ricci C, Scambia G, Capelli G. Long‐term efficacy and safety of human papillomavirus vaccination. International Journal of Womens Health 2014;6(1179‐411 (Electronic), 1179‐411 (Linking)):999‐1010. - PMC - PubMed
Dobson 2013 {published data only}
    1. Dobson SR, McNeil S, Dionne M, Dawar M, Ogilvie G, Krajden M. Immunogenicity of 2 doses of HPV vaccine in younger adolescents vs 3 doses in young women: a randomized clinical trial. JAMA 2013;309(17):1793‐802. - PubMed
Draper 2011 {published data only}
    1. Draper E, Bissett SL, Howell‐Jones R, Edwards D, Munslow G, Soldan K. Neutralization of non‐vaccine human papillomavirus pseudoviruses from the A7 and A9 species groups by bivalent HPV vaccine sera. Vaccine 2011;29(47):8585‐90. - PMC - PubMed
Draper 2013 {published data only}
    1. Draper E, Bissett SL, Howell‐Jones R, Waight P, Soldan K, Jit M. A randomized, observer‐blinded immunogenicity trial of cervarix((R)) and gardasil((R)) human papillomavirus vaccines in 12‐15 year old girls. PLOS One 2013;8(5):e61825. - PMC - PubMed
Einstein 2009 {published data only}
    1. Einstein MH, Baron M, Levin MJ, Chatterjee A, Edwards RP, Zepp F. Comparison of the immunogenicity and safety of Cervarix and Gardasil human papillomavirus (HPV) cervical cancer vaccines in healthy women aged 18 to 45 years. Human Vaccines & Immunotherapeutics 2009;5(10):705‐19. - PubMed
Einstein 2011 {published data only}
    1. Einstein MH, Baron M, Levin MJ, Chatterjee A, Fox B, Scholar S. Comparative immunogenicity and safety of human papillomavirus (HPV) 16/18 vaccine and HPV‐6/11/16/18 vaccine: Follow‐up from months 12 to 24 in a Phase III randomized study of healthy women aged 18 to 45 years. Human Vaccines & Immunotherapeutics 2011;7(12):1343‐58. - PMC - PubMed
Evans 2001 {published data only}
    1. Evans TG, Bonnez W, Rose RC, Koenig S, Demeter L, Suzich JA. A Phase 1 study of a recombinant viruslike particle vaccine against human papillomavirus type 11 in healthy adult volunteers. Journal of Infectious Diseases 2001;183(0022‐1899, 10):1485‐93. - PubMed
Forinash 2011 {published data only}
    1. Forinash AB, Yancey AM, Pitlick JM, Myles TD. Safety of the HPV bivalent and quadrivalent vaccines during pregnancy. Annals of Pharmacotherapy 2011;45(3):1‐5. - PubMed
Garland 2016 {published data only}
    1. Garland SM, Paavonen J, Jaisamrarn U, Naud P, Salmeron J, Chow SN, et al. Prior human papillomavirus‐16/18 AS04‐adjuvanted vaccination prevents recurrent high grade cervical intraepithelial neoplasia after definitive surgical therapy: Post‐hoc analysis from a randomized controlled trial. International Journal of Cancer 2016;139(1097‐0215 (Electronic), 0020‐7136 (Linking), 12):2812‐26. - PMC - PubMed
Giuliano 2007 {published data only}
    1. Giuliano AR, Lazcano‐Ponce E, Villa L, Nolan T, Marchant C, Radley D. Impact of baseline covariates on the immunogenicity of a quadrivalent (types 6, 11, 16, and 18) human papillomavirus virus‐like‐particle vaccine. Journal of Infectious Diseases 2007;196(8):1153‐62. - PubMed
Giuliano 2011 {published data only}
    1. Giuliano AR, Palefsky JM, Goldstone S, Moreira ED, Penny ME, Aranda C. Efficacy of quadrivalent HPV vaccine against HPV infection and disease in males. New England Journal of Medcine 2011;364(5):401‐11. - PMC - PubMed
Giuliano 2015 {published data only}
    1. Giuliano AR, Isaacs‐Soriano K, Torres BN, Abrahamsen M, Ingles DJ, Sirak BA, et al. Immunogenicity and safety of Gardasil among mid‐adult aged men (27 to 45 years) The MAM Study. Vaccine 2015;33(1873‐2518 (Electronic), 0264‐410X (Linking), 42):5640‐6. - PubMed
Goldstone 2013 {published data only}
    1. Goldstone SE, Jessen H, Palefsky JM, Giuliano AR, Moreira ED Jr, Vardas E, et al. Quadrivalent HPV vaccine efficacy against disease related to vaccine and non‐vaccine HPV types in males. Vaccine 2013;31(37):3849‐55. - PubMed
Harro 2001 {published data only}
    1. Harro CD, Pang YY, Roden RB, Hildesheim A, Wang Z, Reynolds MJ. Safety and immunogenicity trial in adult volunteers of a human papillomavirus 16 L1 virus‐like particle vaccine. Journal of the National Cancer Institute 2001;93(4):284‐92. - PubMed
Haupt 2011 {published data only}
    1. Haupt RM, Wheeler CM, Brown DR, Garland SM, Ferris DG, Paavonen JA. Impact of an HPV6/11/16/18 L1 virus‐like particle vaccine on progression to cervical intraepithelial neoplasia in seropositive women with HPV16/18 infection. International Journal of Cancer 2011;129(11):2632‐42. - PubMed
Heijstek 2014 {published data only}
    1. Heijstek MW, Scherpenisse M, Groot N, Tacke C, Schepp RM, Buisman AM, et al. Immunogenicity and safety of the bivalent HPV vaccine in female patients with juvenile idiopathic arthritis: a prospective controlled observational cohort study. Annals of the RheumaticDiseases 2014;73(1468‐2060 (Electronic), 0003‐4967 (Linking), 8):1500‐7. - PubMed
Hernandez‐Avila 2016 {published data only}
    1. Hernandez‐Avila M, Torres‐Ibarra L, Stanley M, Salmeron J, Cruz‐Valdez A, Munoz N, et al. Evaluation of the immunogenicity of the quadrivalent HPV vaccine using 2 versus 3 doses at month 21: An epidemiological surveillance mechanism for alternate vaccination schemes. Human Vaccines & Immunotherapeutics 2016;12(2164‐554X (Electronic), 2164‐5515 (Linking), 1):30‐8. - PMC - PubMed
Herrero 2013 {published data only}
    1. Herrero R, Quint W, Hildesheim A, Gonzalez P, Struijk L, Katki HA. Reduced prevalence of oral human papillomavirus (HPV) 4 years after bivalent HPV vaccination in a randomized clinical trial in Costa Rica. PLOS One 2013;8(7):e68329. - PMC - PubMed
Hildesheim 2007 {published data only}
    1. Hildesheim A, Herrero R, Wacholder S, Rodriguez AC, Solomon D, Bratti MC. Effect of human papillomavirus 16/18 L1 viruslike particle vaccine among young women with preexisting infection: a randomized trial. JAMA 2007;298(7):743‐53. - PubMed
Hillman 2011 {published data only}
    1. Hillman RJ, Giuliano AR, Palefsky JM, Goldstone S, Moreira ED Jr, Vardas E. The immunogenicity of quadrivalent HPV (type 6/11/16/18) vaccine in males aged 16 to 26. Clinical and Vaccine Immunology 2011;19:261‐7. - PMC - PubMed
Joura 2007 {published data only}
    1. Joura EA, Leodolter S, Hernandez‐Avila M, Wheeler CM, Perez G, Koutsky LA. Efficacy of a quadrivalent prophylactic human papillomavirus (types 6, 11, 16, and 18) L1 virus‐like‐particle vaccine against high‐grade vulval and vaginal lesions: a combined analysis of three randomised clinical trials. Lancet 2007;369(9574):1693‐702. - PubMed
Kahn 2013 {published data only}
    1. Kahn JA, Xu J, Kapogiannis BG, Rudy B, Gonin R, Liu N, et al. Immunogenicity and safety of the human papillomavirus 6, 11, 16, 18 vaccine in HIV‐infected young women. Clinical Infectious Diseases 2013;57(5):735‐44. - PMC - PubMed
Kang 2013 {published data only}
    1. Kang WD, Choi HS, Kim SM. Is vaccination with quadrivalent HPV vaccine after loop electrosurgical excision procedure effective in preventing recurrence in patients with high‐grade cervical intraepithelial neoplasia (CIN2‐3)?. Gynecologic Oncology 2013;130(2):264‐8. - PubMed
Khatun 2012 {published data only}
    1. Khatun S, Akram Hussain SM, Chowdhury S, Ferdous J, Hossain F, Begum SR. Safety and immunogenicity profile of human papillomavirus‐16/18 AS04 adjuvant cervical cancer vaccine: a randomized controlled trial in healthy adolescent girls of Bangladesh. Japanese Journal of Clinical Oncology 2012;42(1):36‐41. - PMC - PubMed
Kjaer 2009 {published data only}
    1. Kjaer SK, Sigurdsson K, Iversen OE, Hernandez‐Avila M, Wheeler CM, Perez G, et al. A pooled analysis of continued prophylactic efficacy of quadrivalent human papillomavirus (Types 6/11/16/18) vaccine against high‐grade cervical and external genital lesions. Cancer Prevention Research (Philadelphia, Pa.) 2009;2(1940‐6215 (Electronic), 10):868‐78. - PubMed
Kreimer 2015 {published data only}
    1. Kreimer AR, Sherman ME, Sahasrabuddhe VV, Safaeian M. The case for conducting a randomized clinical trial to assess the efficacy of a single dose of prophylactic HPV vaccines among adolescents. Journal of the National Cancer Institute 2015;107(3 1460‐2105 (Electronic)):1‐4 0027‐8874 (Linking). - PMC - PubMed
Lamontagne 2013 {published data only}
    1. Lamontagne DS, Thiem VD, Huong VM, Tang Y, Neuzil KM. Immunogenicity of quadrivalent HPV vaccine among girls 11 to 13 Years of age vaccinated using alternative dosing schedules: results 29 to 32 months after third dose. Journal of Infectious Diseases 2013;208(8):1325‐34. - PubMed
Lang 2014 {published data only}
    1. Lang Kuhs KA, Gonzalez P, Rodriguez AC, Doorn LJ, Schiffman M, Struijk L, et al. Reduced prevalence of vulvar HPV16/18 infection among women who received the HPV16/18 bivalent vaccine: a nested analysis within the Costa Rica Vaccine Trial. Journal of Infectious Diseases 2014;210(12):1890‐9. - PMC - PubMed
Lazcano‐Ponce 2014 {published data only}
    1. Lazcano‐Ponce E, Stanley M, Munoz N, Torres L, Cruz‐Valdez A, Salmeron J, et al. Overcoming barriers to HPV vaccination: non‐inferiority of antibody response to human papillomavirus 16/18 vaccine in adolescents vaccinated with a two‐dose vs. a three‐dose schedule at 21 months. Vaccine 2014;32(6):725‐32. - PubMed
Lehtinen 2016 {published data only}
    1. Lehtinen M, Eriksson T, Apter D, Hokkanen M, Natunen K, Paavonen J, et al. Safety of the human papillomavirus (HPV)‐16/18 AS04‐adjuvanted vaccine in adolescents aged 12‐15 years: Interim analysis of a large community‐randomized controlled trial. Human Vaccines & Immunotherapeutics 2016;12(2164‐554X (Electronic), 2164‐5515 (Linking), 12):3177‐85. - PMC - PubMed
Leroux‐Roels 2011 {published data only}
    1. Leroux‐Roels G, Haelterman E, Maes C, Levy J, Boever F, Licini L. Randomized trial of the immunogenicity and safety of the Hepatitis B vaccine given in an accelerated schedule coadministered with the human papillomavirus type 16/18 AS04‐adjuvanted cervical cancer vaccine. Clinical Vaccine Immunology 2011;18(9):1510‐8. - PMC - PubMed
Leung 2015 {published data only}
    1. Leung TF, Liu AP, Lim FS, Thollot F, Oh HM, Lee BW, et al. 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. Human Vaccines & Immunotherapeutics 2015;11(2164‐554X (Electronic), 2164‐5515 (Linking), 7):1689‐702. - PMC - PubMed
Li 2012 {published data only}
    1. Li R, Li Y, Radley D, Liu Y, Huang T, Sings HL. Safety and immunogenicity of a vaccine targeting human papillomavirus types 6, 11, 16 and 18: a randomized, double‐blind, placebo‐controlled trial in Chinese males and females. Vaccine 2012;30(28):4284‐91. - PubMed
Lin 2014 {published data only}
    1. Lin CJ, Zimmerman RK, Nowalk MP, Huang HH, Raviotta JM. Randomized controlled trial of two dosing schedules for human papillomavirus vaccination among college age males. Vaccine 2014;32(6):693‐9. - PMC - PubMed
Lu 2011 {published data only}
    1. Lu B, Kumar A, Castellsague X, Giuliano AR. Efficacy and safety of prophylactic vaccines against cervical HPV infection and diseases among women: a systematic review & meta‐analysis. BMC Infectious Disease 2011;11(1):13. - PMC - PubMed
Luna 2013 {published data only}
    1. Luna J, Plata M, Gonzalez M, Correa A, Maldonado I, Nossa C. Long‐term follow‐up observation of the safety, immunogenicity, and effectiveness of Gardasil in adult women. PLOS One 2013;8(12):e83431. - PMC - PubMed
Malagon 2012 {published data only}
    1. Malagon T, Drolet M, Boily MC, Franco EL, Jit M, Brisson J. Cross‐protective efficacy of two human papillomavirus vaccines: a systematic review and meta‐analysis. Lancet Infectious Diseases 2012;12(10):781‐9. - PubMed
McCormack 2011 {published data only}
    1. McCormack PL, Joura EA. Spotlight on quadrivalent human papillomavirus (types 6, 11, 16, 18) recombinant vaccine(Gardasil®) in the prevention of premalignant genital lesions, genital cancer, and genital warts in women. BioDrugs 2011;25(5):339‐43. - PubMed
McKeage 2011 {published data only}
    1. McKeage K, Romanowski B. Spotlight on AS04‐adjuvanted human papillomavirus (HPV) types 16 and 18 vaccine (Cervarix®). BioDrugs 2011;25(4):265‐9. - PubMed
Money 2016 {published data only}
    1. Money DM, Moses E, Blitz S, Vandriel SM, Lipsky N, Walmsley SL, et al. HIV viral suppression results in higher antibody responses in HIV‐positive women vaccinated with the quadrivalent human papillomavirus vaccine. Vaccine 2016;34(40):4799‐806. - PubMed
Moreira 2011 {published data only}
    1. Moreira ED, Palefsky JM, Giuliano AR, Goldstone S, Aranda C, Jessen H. Safety and reactogenicity of a quadrivalent human papillomavirus (types 6, 11, 16, 18) L1 viral‐like‐particle vaccine in older adolescents and young adults. Human Vaccines & Immunotherapeutics 2011;7(7):768‐75. - PMC - PubMed
Nakalembe 2015 {published data only}
    1. Nakalembe M, Mirembe FM, Banura C. Vaccines against human papillomavirus in low and middle income countries: a review of safety, immunogenicity and efficacy. Infectious Agents and Cancer 2015;10(1750‐9378 (Electronic), 1750‐9378 (Linking)):17. - PMC - PubMed
Nelson 2013 {published data only}
    1. Nelson EA, Lam HS, Choi KC, Ho WCS, Fung LWE, Cheng FWT. A pilot randomized study to assess immunogenicity, reactogenicity, safety and tolerability of two human papillomavirus vaccines administered intramuscularly and intradermally to females aged 18‐26 years. Vaccine 2013;31(34):3452‐60. - PubMed
Neuzil 2011 {published data only}
    1. Neuzil KM, Canh DG, Thiem VD, Janmohamed A, Huong VM, Tang Y. Immunogenicity and reactogenicity of alternative schedules of HPV vaccine in Vietnam: a cluster randomized noninferiority trial. JAMA 2011;305(14):1424‐31. - PubMed
Olsson 2009 {published data only}
    1. Olsson SE, Kjaer SK, Sigurdsson K, Iversen OE, Hernandez‐Avila M, Wheeler CM, et al. Evaluation of quadrivalent HPV 6/11/16/18 vaccine efficacy against cervical and anogenital disease in subjects with serological evidence of prior vaccine type HPV infection. Human Vaccines 2009;5(1554‐8619 (Electronic), 10):696‐704. - PubMed
Palefsky 2011 {published data only}
    1. Palefsky JM, Giuliano AR, Goldstone SE, Moreira ED Jr, Aranda C, Jessen H. HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. New England Journal of Medicine 2011;365(17):1576‐85. - PubMed
Pedersen 2007 {published data only}
    1. Pedersen C, Petaja T, Strauss G, Rumke HC, Poder A, Richardus JH, et al. Immunization of early adolescent females with human papillomavirus type 16 and 18 L1 virus‐like particle vaccine containing AS04 adjuvant. Journal of Adolescent Health 2007;40(6):564‐71. - PubMed
Perez 2008 {published data only}
    1. Perez G, Lazcano‐Ponce E, Hernandez‐Avila M, Garcia PJ, Munoz N, Villa LL. Safety, immunogenicity, and efficacy of quadrivalent human papillomavirus (types 6, 11, 16, 18) L1 virus‐like‐particle vaccine in Latin American women. International Journal of Cancer 2008;122(6):1311‐8. - PubMed
Petaja 2009 {published data only}
    1. Petaja T, Keranen H, Karppa T, Kawa A, Lantela S, Siitari‐Mattila M. Immunogenicity and safety of human papillomavirus (HPV)‐16/18 AS04‐adjuvanted vaccine in healthy boys aged 10‐18 years. Journal of Adolescent Health 2009;44(1):33‐40. - PubMed
Petaja 2011 {published data only}
    1. Petaja T, Pedersen C, Poder A, Strauss G, Catteau G, Thomas F, et al. Long‐term persistence of systemic and mucosal immune response to HPV‐16/18 AS04‐adjuvanted vaccine in preteen/adolescent girls and young women. International Journal of Cancer 2011;129(9):2147‐57. - PubMed
Poland 2005 {published data only}
    1. Poland GA, Jacobson RM, Koutsky LA, Tamms GM, Railkar R, Smith JF. Immunogenicity and reactogenicity of a novel vaccine for human papillomavirus 16: a 2‐year randomized controlled clinical trial. Mayo Clinic Proceedings 2005;80(5):601‐10. - PubMed
Puthanakit 2016 {published data only}
    1. Puthanakit T, Huang LM, Chiu CH, Tang RB, Schwarz TF, Esposito S, et al. Randomized open trial comparing 2‐dose regimens of the human papillomavirus 16/18 AS04‐adjuvanted vaccine in girls aged 9‐14 years versus a 3‐dose regimen in women aged 15‐25 years. Journal of Infectious Diseases 2016;214(4):525‐36. - PMC - PubMed
Ramanakumar 2016 {published data only}
    1. Ramanakumar AV, Naud P, Roteli‐Martins CM, Carvalho NS, Borba PC, Teixeira JC, et al. Incidence and duration of type‐specific human papillomavirus infection in high‐risk HPV‐naive women: results from the control arm of a phase II HPV‐16/18 vaccine trial. BMJ Open. 2016;6(2044‐6055 (Electronic), 2044‐6055 (Linking), 8):e011371. - PMC - PubMed
Read 2011 {published data only}
    1. Read TR, Hocking JS, Chen MY, Donovan B, Bradshaw CS, Fairley CK. The near disappearance of genital warts in young women 4 years after commencing a national human papillomavirus (HPV) vaccination programme. Sexually Transmitted Infections 2011;87(7):544‐7. - PubMed
Reisinger 2007 {published data only}
    1. Reisinger KS, Block SL, Lazcano‐Ponce E, Samakoses R, Esser MT, Erick J, et al. Safety and persistent immunogenicity of a quadrivalent human papillomavirus types 6, 11, 16, 18 L1 virus‐like particle vaccine in preadolescents and adolescents: a randomized controlled trial. Pediatric Infectious Disease Journal 2007;26(3):201‐9. - PubMed
Reisinger 2010 {published data only}
    1. Reisinger KS, Block SL, Collins‐Ogle M, Marchant C, Catlett M, Radley D, et al. Safety, tolerability, and immunogenicity of gardasil given concomitantly with Menactra and Adacel. Pediatrics 2010;125(6):1142‐51. - PubMed
Romanowski 2016 {published data only}
    1. Romanowski B, Schwarz TF, Ferguson L, Peters K, Dionne M, Behre U, et al. Sustained immunogenicity of the HPV‐16/18 AS04‐adjuvanted vaccine administered as a two‐dose schedule in adolescent girls: Five‐year clinical data and modeling predictions from a randomized study. Human Vaccines & Immunotherapeutics 2016;12(2164‐554X (Electronic), 2164‐5515 (Linking), 1):20‐9. - PMC - PubMed
Rowhani‐Rahbar 2012 {published data only}
    1. Rowhani‐Rahbar A, Alvarez FB, Bryan JT, Hughes JP, Hawes SE, Weiss NS. Evidence of immune memory 8.5 years following administration of a prophylactic human papillomavirus type 16 vaccine. Journal of Clinical Virology 2012;53(3):239‐43. - PMC - PubMed
Safaeian 2013 {published data only}
    1. Safaeian M, Kemp TJ, Pan DY, Porras C, Rodriguez AC, Schiffman M, et al. Cross‐protective vaccine efficacy of the bivalent HPV vaccine against HPV31 is associated with humoral immune responses: results from the Costa Rica Vaccine Trial. Human Vaccines & Immunotherapeutics 2013;9(7):1399‐406. - PMC - PubMed
Schwarz 2008 {published data only}
    1. Schwarz TF, Leo O. Immune response to human papillomavirus after prophylactic vaccination with AS04‐adjuvanted HPV‐16/18 vaccine: improving upon nature. Gynecologic Oncology 2008;110(3 Suppl 1):S1‐10. - PubMed
Schwarz 2009 {published data only}
    1. Schwarz TF, Spaczynski M, Schneider A, Wysocki J, Galaj A, Perona P. Immunogenicity and tolerability of an HPV‐16/18 AS04‐adjuvanted prophylactic cervical cancer vaccine in women aged 15‐55 years. Vaccine 2009;27(4):581‐7. - PubMed
Schwarz 2010 {published data only}
    1. Schwarz TF, Kocken M, Petaja T, Einstein MH, Spaczynski M, Louwers JA. Correlation between levels of human papillomavirus (HPV) 16 and 18 antibodies in serum and cervicovaginal secretions in girls and women vaccinated with the HPV‐16/18 AS04‐adjuvanted vaccine. Human Vaccine & Immunotherapeutics 2010;6(12):1054‐61. - PubMed
Schwarz 2011 {published data only}
    1. Schwarz TF, Spaczynski M, Schneider A, Wysocki J, Galaj A, Schulze K. Persistence of immune response to HPV‐16/18 AS04‐adjuvanted cervical cancer vaccine in women aged 15‐55 years. Human Vaccines & Immunotherapeutics 2011;7(9):958‐65. - PMC - PubMed
Schwarz 2014 {published data only}
    1. Schwarz TF, Huang LM, Lin TY, Wittermann C, Panzer F, Valencia A, et al. Long‐term immunogenicity and safety of the HPV‐16/18 AS04‐adjuvanted vaccine in 10‐ to 14‐year‐old girls: open 6‐year follow‐up of an initial observer‐blinded, randomized trial. Pediatric Infectious Disease Journal 2014;33(1532‐0987 (Electronic), 0891‐3668 (Linking), 12):1255‐61. - PubMed
Sengupta 2011 {published data only}
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