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Original Research

Post-hoc analysis from phase III trials of human papillomavirus vaccines: considerations on impact on non-vaccine types

, ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon
Pages 309-322 | Received 28 Aug 2018, Accepted 04 Feb 2019, Published online: 04 Mar 2019

References

  • de Martel C , Ferlay J , Franceschi S , et al . Global burden of cancers attributable to infections in 2008: a review and synthetic analysis . Lancet Oncol . 2012 ; 13 ( 6 ): 607 – 615 .
  • WHO. World Health Organization . Human Papillomavirus (HPV) and cervical cancer. Key facts. 2018 ; 2018 [cited 2018 Jul 27] . Available from : http://www.who.int/mediacentre/factsheets/fs380/en/#
  • European Medicines Agency (EMA) . Gardasil 9, European summary of product characteristics 2015 . 2015 July .
  • European Medicines Agency (EMA) . Gardasil, European summary of product characteristics 2014 . 2014 August .
  • Deschuyteneer M , Elouahabi A , Plainchamp D , et al . Molecular and structural characterization of the L1 virus-like particles that are used as vaccine antigens in CervarixTM, the AS04-adjuvanted HPV-16 and -18 cervical cancer vaccine . Hum Vaccin Immunother . 2010 ; 6 ( 5 ): 1 – 13 .
  • Einstein MH , Takacs P , Chatterjee A , 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 ( 12 ): 3435 – 3445 .
  • Draper E , Bissett SL , Howell-Jones R , et al . A randomized, observer-blinded immunogenicity trial of cervarix® and gardasil® human papillomavirus vaccines in 12–15 year old girls . PLoS One . 2013 ; 8 ( 5 ): e61825 .
  • Munoz N , Kjaer SK , Sigurdsson K , et al . Impact of human papillomavirus (HPV)-6/11/16/18 vaccine on all HPV-associated genital diseases in young women . J Natl Cancer Inst . 2010 ; 102 ( 5 ): 325 – 339 .
  • Joura EA , Giuliano AR , Iversen OE , et al . A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women . N Engl J Med . 2015 ; 372 ( 8 ): 711 – 723 .
  • Lehtinen M , Paavonen J , Wheeler CM , 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 ( 1 ): 89 – 99 .
  • Stanley M. Immune responses to human papillomavirus . Vaccine . 2006 ; 24 ( Suppl. 1 ): S16 – S22 .
  • Kavanagh K , Pollock KG , Cuschieri K , et al . Changes in the prevalence of human papillomavirus following a national bivalent human papillomavirus vaccination programme in Scotland: a 7-year cross-sectional study . Lancet Infect Dis . 2017 ; 17 ( 12 ): 1293 – 1302 .
  • Mesher D , Panwar K , Thomas SL , et al . The impact of the national HPV vaccination program in England using the bivalent HPV vaccine: surveillance of type-specific HPV in young females, 2010–2016 . J Infect Dis . 2018 ; 218 : 911–921 .
  • Wheeler CM , Castellsague X , Garland SM , et al . Cross-protective efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by non-vaccine oncogenic HPV types: end-of-study (4-year) analysis of the randomised, double-blind PATRICIA trial . Lancet Oncol . 2012 ; 13 ( 1 ): 100 – 110 .
  • Brown DR , Kjaer SK , Sigurdsson K , et al . The impact of quadrivalent human papillomavirus (HPV; Types 6, 11, 16, and 18) L1 virus-like particle vaccine on infection and disease due to oncogenic nonvaccine HPV types in generally HPV-naive women aged 16–26 years . J Infect Dis . 2009 ; 199 ( 7 ): 926 – 935 .
  • Pratt D , Goldenthal K , Geber A . Preventive human papillomavirus (HPV) vaccines – regulatory briefing document on endpoints, vaccines and related biological products advisory committee meeting . Bethesda (MD) ; 2001 .
  • Lehtinen M , Dillner J . Clinical trials of human papillomavirus vaccines and beyond . Nat Rev Clin Oncol . 2013 ; 10 ( 7 ): 400 – 410 .
  • Di Mario S , Basevi V , Lopalco PL , et al . Are the two human papillomavirus vaccines really similar? A systematic review of available evidence: efficacy of the two vaccines against HPV . J Immunol Res . 2015 ; 2015 : 435141 .
  • Arbyn M , Xu L , Simoens C , et al . Prophylactic vaccination against human papillomaviruses to prevent cervical cancer and its precursors . Cochrane Database Syst Rev . 2018 ; 5 : CD009069 .
  • Joura EA , Ault KA , Bosch FX , et al . Attribution of 12 high-risk human papillomavirus genotypes to infection and cervical disease . Cancer Epidemiol Biomarkers Prev . 2014 ; 23 ( 10 ): 1997 – 2008 .
  • Pollock K. Update on Scottish HPV vaccination program [cited 2018 Jul 27] . Available from : https://www.hse.ie/eng/health/Immunisation/hcpinfo/conference/hpv173.pdf
  • Brotherton JML , Malloy M , Budd AC , et al . Effectiveness of less than three doses of quadrivalent human papillomavirus vaccine against cervical intraepithelial neoplasia when administered using a standard dose spacing schedule: observational cohort of young women in Australia . Papillomavirus Res . 2015 ; 1 : 59 – 73 .
  • Kim J , Bell C , Sun M , et al . Effect of human papillomavirus vaccination on cervical cancer screening in Alberta . Can Med Assoc J . 2016 ; 188 ( 12 ): E281 – 8 .
  • Sykes P , Innes C , Simcock B , et al . What is the impact of HPV vaccination program on natural history of high grade squamous intraepithelial cervical lesions in New Zealand? Abstract No. FC 03-08 . Presented at EUropean Research Organisation on Genital Infection and Neoplasia (EUROGIN) ; 2017 Oct 8–11 . [cited 2018 Jul 27] . Available from : https://www.eurogin.com/images/PDF/EUROGIN-2017.pdf
  • Roden RBS , Stern PL . Opportunities and challenges for human papillomavirus vaccination in cancer . Nat Rev Cancer . 2018 ; 18 ( 4 ): 240 – 254 .
  • Schiller J , Lowy D . Explanations for the high potency of HPV prophylactic vaccines . Vaccine . 2018 ; 36 ( 32Pt A ): 4768 – 4773 .
  • Arbyn M . Effects of quadrivalent human papillomavirus vaccination . Lancet . 2007 ; 370 ( 9592 ): 1031 – 1032 . author reply 1032-3 .
  • Callegari ET , Tabrizi SN , Pyman J , et al . How best to interpret mixed human papillomavirus genotypes in high-grade cervical intraepithelial neoplasia lesions . Vaccine . 2014 ; 32 ( 32 ): 4082 – 4088 .
  • van der Marel J , Berkhof J , Ordi J , et al . Attributing oncogenic human papillomavirus genotypes to high-grade cervical neoplasia: which type causes the lesion? Am J Surg Pathol . 2015 ; 39 ( 4 ): 496 – 504 .
  • Munoz N , Manalastas R Jr. , Pitisuttithum P , et al . Safety, immunogenicity, and efficacy of quadrivalent human papillomavirus (types 6, 11, 16, 18) recombinant vaccine in women aged 24–45 years: a randomised, double-blind trial . Lancet . 2009 ; 373 ( 9679 ): 1949 – 1957 .
  • Bautista OM , Luxembourg A . Deconstructing the measure of vaccine efficacy against disease irrespective of HPV in HPV vaccine clinical trials . Contemp Clin Trials . 2016 ; 47 : 254 – 258 .
  • Folschweiller N , Berlaimont V , Skinner SR , et al . Letter to the editor in response to O.M. Bautista, A. Luxembourg. Deconstructing the measure of vaccine efficacy against disease irrespective of HPV in HPV vaccine clinical trials . Contemp Clin Trials . 2017 ; 47 ( 2016 ): 254 – 258 . Contemp Clin Trials. 2017;54:106–7 .
  • Dragalin V , Fedorov V , Cheuvart B . Statistical approaches to establishing vaccine safety . Stat Med . 2002 ; 21 ( 6 ): 877 – 893 .
  • Giuliano . Efficacy of a novel 9-valent HPV L1 vaccine against disease irrespective of HPV type. Abstract PHPD0405 . Presented at the 29th International Papillomavirus Conference ; 2014 Aug 20–25 ; Seattle, Washington .
  • Hartwig S , Baldauf JJ , Dominiak-Felden GÃ , et al . Estimation of the epidemiological burden of HPV-related anogenital cancers, precancerous lesions, and genital warts in women and men in Europe: potential additional benefit of a nine-valent second generation HPV vaccine compared to first generation HPV vaccines . Papillomavirus Res . 2015 ; 1 : 90 – 100 .
  • Donken R , King AJ , Bogaards JA , et al . High effectiveness of the bivalent human papillomavirus (HPV) vaccine against incident and persistent HPV infections up to 6 years after vaccination in young Dutch women . J Infect Dis . 2018 ; 217 ( 10 ): 1579 – 1589 .
  • Lehtinen M , Soderlund-Strand A , Vanska S , et al . Impact of gender-neutral or girls-only vaccination against human papillomavirus-results of a community-randomized clinical trial (I) . Int J Cancer . 2018 ; 142 ( 5 ): 949 – 958 .
  • Mesher D , Soldan K , Lehtinen M , et al . Population-level effects of human papillomavirus vaccination programs on infections with nonvaccine genotypes . Emerg Infect Dis . 2016 ; 22 ( 10 ): 1732 – 1740 .
  • Canvin M , Sinka K , Hughes G , et al . Decline in genital warts diagnoses among young women and young men since the introduction of the bivalent HPV (16/18) vaccination programme in England: an ecological analysis . Sex Transm Infect . 2017 ; 93 ( 2 ): 125 – 128 .
  • Faust H , Toft L , Sehr P , et al . Human papillomavirus neutralizing and cross-reactive antibodies induced in HIV-positive subjects after vaccination with quadrivalent and bivalent HPV vaccines . Vaccine . 2016 ; 34 ( 13 ): 1559 – 1565 .
  • Scherpenisse M , Schepp RM , Mollers M , et al . Characteristics of HPV-specific antibody responses induced by infection and vaccination: cross-reactivity, neutralizing activity, avidity and IgG subclasses . PLoS One . 2013 ; 8 ( 9 ): e74797 .
  • Opalka DW , Matys K , Green T , et al . Development of a multiplexed HPV L1 viruslike particle type specific immunoglobulin subclass and isotyping assay . FASEB J . 2008 ; 22 ( Meeting Abstract Supplement ): 859.14 .
  • Ruiz W , McClements WL , Jansen KU , et al . Kinetics and isotype profile of antibody responses in rhesus macaques induced following vaccination with HPV 6, 11, 16 and 18 L1-virus-like particles formulated with or without Merck aluminum adjuvant . J Immune Based Ther Vaccines . 2005 ; 3 ( 1 ): 2 .
  • Arnold KB , Chung AW . Prospects from systems serology research . Immunology . 2018 ; 153 ( 3 ): 279 – 289 .
  • Iwasaki A . Exploiting mucosal immunity for antiviral vaccines . Annu Rev Immunol . 2016 ; 34 : 575 – 608 .
  • Chung AW , Ghebremichael M , Robinson H , et al . Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines . Sci Transl Med . 2014 ; 6 ( 228 ): 228ra38 .
  • Crescioli S , Correa I , Karagiannis P , et al . IgG4 characteristics and functions in cancer immunity . Curr Allergy Asthma Rep . 2016 ; 16 ( 1 ): 7 .
  • Ackerman ME , Barouch DH , Alter G . Systems serology for evaluation of HIV vaccine trials . Immunol Rev . 2017 ; 275 ( 1 ): 262 – 270 .
  • Pinto LA , Edwards J , Castle PE , et al . Cellular immune responses to human papillomavirus (HPV)-16 L1 in healthy volunteers immunized with recombinant HPV-16 L1 virus-like particles . J Infect Dis . 2003 ; 188 ( 2 ): 327 – 338 .
  • Szarewski A , Skinner SR , Garland SM , et al . Efficacy of the HPV-16/18 AS04-adjuvanted vaccine against low-risk HPV types (PATRICIA randomized trial): an unexpected observation . J Infect Dis . 2013 ; 208 ( 9 ): 1391 – 1396 .
  • Stanley M . Prophylactic HPV vaccines . J Clin Pathol . 2007 ; 60 ( 9 ): 961 – 965 .
  • Mirkovic J , Howitt BE , Roncarati P , et al . Carcinogenic HPV infection in the cervical squamo-columnar junction . J Pathol . 2015 ; 236 ( 3 ): 265 – 271 .
  • Herfs M , Yamamoto Y , Laury A , et al . A discrete population of squamocolumnar junction cells implicated in the pathogenesis of cervical cancer . Proc Natl Acad Sci USA . 2012 ; 109 ( 26 ): 10516 – 10521 .
  • Torres-Poveda K , Bahena-Roman M , Madrid-Gonzalez C , et al . Role of IL-10 and TGF-beta1 in local immunosuppression in HPV-associated cervical neoplasia . World J Clin Oncol . 2014 ; 5 ( 4 ): 753 – 763 .
  • Didierlaurent AM , Morel S , Lockman L , et al . AS04, an aluminum salt- and TLR4 agonist-based adjuvant system, induces a transient localized innate immune response leading to enhanced adaptive immunity . J Immunol . 2009 ; 183 ( 10 ): 6186 – 6197 .
  • Tobery TW , Smith JF , Kuklin N , et al . Effect of vaccine delivery system on the induction of HPV16L1-specific humoral and cell-mediated immune responses in immunized rhesus macaques . Vaccine . 2003 ; 21 ( 13–14 ): 1539 – 1547 .
  • Herrin DM , Coates EE , Costner PJ , et al . Comparison of adaptive and innate immune responses induced by licensed vaccines for human papillomavirus . Hum Vaccin Immunother . 2014 ; 10 ( 12 ): 3446 – 3454 .
  • Fausch SC , Da Silva DM , Kast WM . Heterologous papillomavirus virus-like particles and human papillomavirus virus-like particle immune complexes activate human langerhans cells . Vaccine . 2005 ; 23 ( 14 ): 1720 – 1729 .
  • Szarewski A , Poppe WA , Skinner SR , et al . Efficacy of the human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine in women aged 15–25 years with and without serological evidence of previous exposure to HPV-16/18 . Int J Cancer . 2012 ; 131 ( 1 ): 106 – 116 .
  • Chabeda A , Yanez Romana JR , Lamprecht R , et al . Therapeutic vaccines for high-risk HPV-associated diseases . Papillomavirus Res . 2017 ; 5 : 46 – 58 .
  • Da Silva AR , Babor M , Carpenter C , et al . Th1/Th17 polarization persists following whole-cell pertussis vaccination despite repeated acellular boosters . J Clin Invest . 2018 ; 128 ( 9 ): 3853 – 3865 .
  • Sin JI , Bagarazzi M , Pachuk C , et al . DNA priming-protein boosting enhances both antigen-specific antibody and Th1-type cellular immune responses in a murine herpes simplex virus-2 gD vaccine model . DNA Cell Biol . 1999 ; 18 ( 10 ): 771 – 779 .

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