Human Papillomavirus Vaccine Efficacy and Effectiveness against Cancer

Supitcha Kamolratanakul, Punnee Pitisuttithum, Supitcha Kamolratanakul, Punnee Pitisuttithum

Abstract

Human papillomavirus (HPV) is the most common sexually transmitted infection, with 15 HPV types related to cervical, anal, oropharyngeal, penile, vulvar, and vaginal cancers. However, cervical cancer remains one of the most common cancers in women, especially in developing countries. Three HPV vaccines have been licensed: bivalent (Cervarix, GSK, Rixensart, Belgium), quadrivalent (Merck, Sharp & Dome (Merck & Co, Whitehouse Station, NJ, USA)), and nonavalent (Merck, Sharp & Dome (Merck & Co, Whitehouse Station, NJ, USA)). The current HPV vaccine recommendations apply to 9 years old and above through the age of 26 years and adults aged 27-45 years who might be at risk of new HPV infection and benefit from vaccination. The primary target population for HPV vaccination recommended by the WHO is girls aged 9-14 years, prior to their becoming sexually active, to undergo a two-dose schedule and girls ≥ 15 years of age, to undergo a three-dose schedule. Safety data for HPV vaccines have indicated that they are safe. The most common adverse side-effect was local symptoms. HPV vaccines are highly immunogenic. The efficacy and effectiveness of vaccines has been remarkably high among young women who were HPV seronegative before vaccination. Vaccine efficacy was lower among women regardless of HPV DNA when vaccinated and among adult women. Comparisons of the efficacy of bivalent, quadrivalent, and nonavalent vaccines against HPV 16/18 showed that they are similar. However, the nonavalent vaccine can provide additional protection against HPV 31/33/45/52/58. In a real-world setting, the notable decrease of HPV 6/11/16/18 among vaccinated women compared with unvaccinated women shows the vaccine to be highly effective. Moreover, the direct effect of the nonavalent vaccine with the cross-protection of bivalent and quadrivalent vaccines results in the reduction of HPV 6/11/16/18/31/33/45/52/58. HPV vaccination has been shown to provide herd protection as well. Two-dose HPV vaccine schedules showed no difference in seroconversion from three-dose schedules. However, the use of a single-dose HPV vaccination schedule remains controversial. For males, the quadrivalent HPV vaccine possibly reduces the incidence of external genital lesions and persistent infection with HPV 6/11/16/18. Evidence regarding the efficacy and risk of HPV vaccination and HIV infection remains limited. HPV vaccination has been shown to be highly effective against oral HPV type 16/18 infection, with a significant percentage of participants developing IgG antibodies in the oral fluid post vaccination. However, the vaccines' effectiveness in reducing the incidence of and mortality rates from HPV-related head and neck cancers should be observed in the long term. In anal infections and anal intraepithelial neoplasia, the vaccines demonstrate high efficacy. While HPV vaccines are very effective, screening for related cancers, as per guidelines, is still recommended.

Keywords: HPV vaccine; cervical cancer; human papillomavirus (HPV); other HPV-related cancers; vaccine effectiveness; vaccine efficacy.

Conflict of interest statement

The authors declare no conflict of interest.

References

    1. Cutts F.T., Franceschi S., Goldie S., Castellsague X., de Sanjose S., Garnett G., Edmunds W.J., Claeys P., Goldenthal K.L., Harper D.M., et al. Human papillomavirus and HPV vaccines: A review. Bull. World Health Organ. 2007;85:719–726. doi: 10.2471/BLT.06.038414.
    1. HPV and Cancer. [(accessed on 23 October 2021)]; Available online: .
    1. Zhang Q., Zheng R., Fu Y., Mu Q., Li J. Mental health consequences during alerting situations and recovering to a new normal of coronavirus epidemic in 2019: A cross-sectional study based on the affected population. BMC Public Health. 2021;21:1499. doi: 10.1186/s12889-021-11550-w.
    1. Cancer Stat Facts. [(accessed on 23 October 2021)]; Available online: .
    1. Basu P., Malvi S.G., Joshi S., Bhatla N., Muwonge R., Lucas E., Verma Y., Esmy P.O., Poli U.R.R., Shah A., et al. Vaccine efficacy against persistent human papillomavirus (HPV) 16/18 infection at 10 years after one, two, and three doses of quadrivalent HPV vaccine in girls in India: A multicentre, prospective, cohort study. Lancet Oncol. 2021;22:1518–1529. doi: 10.1016/S1470-2045(21)00453-8.
    1. Working Group on potential contribution of Human Papillomavirus (HPV) vaccines and immunization towards cervical cancer elimination Strategic Advisory Group of Experts (SAGE) on Immunizationa, WHO. [(accessed on 10 October 2021)]. Available online: .
    1. Kjaer S.K., Dehlendorff C., Belmonte F., Baandrup L. Real-World Effectiveness of Human Papillomavirus Vaccination Against Cervical Cancer. J. Natl. Cancer Inst. 2021;113:1329–1335. doi: 10.1093/jnci/djab080.
    1. Lei J., Ploner A., Elfström K.M., Wang J., Roth A., Fang F., Sundström K., Dillner J., Sparén P. HPV Vaccination and the Risk of Invasive Cervical Cancer. N. Engl. J. Med. 2020;383:1340–1348. doi: 10.1056/NEJMoa1917338.
    1. Global Strategy to Accelerate the Elimination of Cervical Cancer as a Public Health Problem. [(accessed on 27 April 2021)]. Available online: .
    1. Weekly Epidemiological Record. [(accessed on 23 October 2021)]. Available online: .
    1. Radley D., Saah A., Stanley M. Persistent infection with human papillomavirus 16 or 18 is strongly linked with high-grade cervical disease. Hum. Vaccines Immunother. 2016;12:768–772. doi: 10.1080/21645515.2015.1088616.
    1. Regional Office for South-East Asia Accelerating the Elimination of Cervical Cancer as a Global Public Health Problem. 2019. [(accessed on 12 October 2021)]. Available online: .
    1. Pinto L.A., Dillner J., Beddows S., Unger E.R. Immunogenicity of HPV prophylactic vaccines: Serology assays and their use in HPV vaccine evaluation and development. Vaccine. 2018;36:4792–4799. doi: 10.1016/j.vaccine.2017.11.089.
    1. Meites E., Szilagyi P.G., Chesson H.W., Unger E.R., Romero J.R., Markowitz L.E. Human Papillomavirus Vaccination for Adults: Updated Recommendations of the Advisory Committee on Immunization Practices. MMWR Morb. Mortal. Wkly. Rep. 2019;68:698–702. doi: 10.15585/mmwr.mm6832a3.
    1. Arbyn M., Xu L., Simoens C., Martin-Hirsch P.P. Prophylactic vaccination against human papillomaviruses to prevent cervical cancer and its precursors. Cochrane Database Syst. Rev. 2018;5:Cd009069. doi: 10.1002/14651858.CD009069.pub3.
    1. Safety of HPV Vaccines. [(accessed on 23 October 2021)]. Available online: .
    1. HPV Vaccine Safety and Effectiveness. [(accessed on 23 October 2021)]; Available online: .
    1. Gee J., Naleway A., Shui I., Baggs J., Yin R., Li R., Kulldorff M., Lewis E., Fireman B., Daley M.F., et al. Monitoring the safety of quadrivalent human papillomavirus vaccine: Findings from the Vaccine Safety Datalink. Vaccine. 2011;29:8279–8284. doi: 10.1016/j.vaccine.2011.08.106.
    1. Bonde U., Joergensen J.S., Lamont R.F., Mogensen O. Is HPV vaccination in pregnancy safe? Hum. Vaccines Immunother. 2016;12:1960–1964. doi: 10.1080/21645515.2016.1160178.
    1. 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. 2014;23:456–465. doi: 10.1002/pds.3593.
    1. Villa A., Patton L.L., Giuliano A.R., Estrich C.G., Pahlke S.C., O’Brien K.K., Lipman R.D., Araujo M.W.B. Summary of the evidence on the safety, efficacy, and effectiveness of human papillomavirus vaccines: Umbrella review of systematic reviews. J. Am. Dent. Assoc. 2020;151:245–254. doi: 10.1016/j.adaj.2019.10.010.
    1. Martínez-Lavín M., Amezcua-Guerra L. Erratum to: Serious adverse events after HPV vaccination: A critical review of randomized trials and post-marketing case series. Clin. Rheumatol. 2017;36:2397. doi: 10.1007/s10067-017-3782-7.
    1. Donahue J.G., Kieke B.A., Lewis E.M., Weintraub E.S., Hanson K.E., McClure D.L., Vickers E.R., Gee J., Daley M.F., DeStefano F., et al. Near Real-Time Surveillance to Assess the Safety of the 9-Valent Human Papillomavirus Vaccine. Pediatrics. 2019;144 doi: 10.1542/peds.2019-1808.
    1. Shimabukuro T.T., Su J.R., Marquez P.L., Mba-Jonas A., Arana J.E., Cano M.V. Safety of the 9-Valent Human Papillomavirus Vaccine. Pediatrics. 2019;144:e20191791. doi: 10.1542/peds.2019-1791.
    1. 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;26:6630–6638. doi: 10.1016/j.vaccine.2008.09.049.
    1. Yih W.K., Greene S.K., Zichittella L., Kulldorff M., Baker M.A., de Jong J.L., Gil-Prieto R., Griffin M.R., Jin R., Lin N.D., et al. Evaluation of the risk of venous thromboembolism after quadrivalent human papillomavirus vaccination among US females. Vaccine. 2016;34:172–178. doi: 10.1016/j.vaccine.2015.09.087.
    1. Donegan K., Beau-Lejdstrom R., King B., Seabroke S., Thomson A., Bryan P. Bivalent human papillomavirus vaccine and the risk of fatigue syndromes in girls in the UK. Vaccine. 2013;31:4961–4967. doi: 10.1016/j.vaccine.2013.08.024.
    1. Grimaldi-Bensouda L., Guillemot D., Godeau B., Bénichou J., Lebrun-Frenay C., Papeix C., Labauge P., Berquin P., Penfornis A., Benhamou P.Y., et al. Autoimmune disorders and quadrivalent human papillomavirus vaccination of young female subjects. J. Intern. Med. 2014;275:398–408. doi: 10.1111/joim.12155.
    1. Miranda S., Chaignot C., Collin C., Dray-Spira R., Weill A., Zureik M. Human papillomavirus vaccination and risk of autoimmune diseases: A large cohort study of over 2million young girls in France. Vaccine. 2017;35:4761–4768. doi: 10.1016/j.vaccine.2017.06.030.
    1. Willame C., Rosillon D., Zima J., Angelo M.G., Stuurman A.L., Vroling H., Boggon R., Bunge E.M., Pladevall-Vila M., Baril L. Risk of new onset autoimmune disease in 9- to 25-year-old women exposed to human papillomavirus-16/18 AS04-adjuvanted vaccine in the United Kingdom. Hum. Vaccines Immunother. 2016;12:2862–2871. doi: 10.1080/21645515.2016.1199308.
    1. Rosillon D., Willame C., Tavares Da Silva F., Guignard A., Caterina S., Welby S., Struyf F. Meta-analysis of the risk of autoimmune thyroiditis, Guillain-Barré syndrome, and inflammatory bowel disease following vaccination with AS04-adjuvanted human papillomavirus 16/18 vaccine. Pharm. Drug Saf. 2020;29:1159–1167. doi: 10.1002/pds.5063.
    1. Stanley M.A., Sudenga S.L., Giuliano A.R. Alternative dosage schedules with HPV virus-like particle vaccines. Expert Rev. Vaccines. 2014;13:1027–1038. doi: 10.1586/14760584.2014.935767.
    1. Hu Y., Zhang X., He Y., Ma Z., Xie Y., Lu X., Xu Y., Zhang Y., Jiang Y., Xiao H., et al. Long-term persistence of immune response to the AS04-adjuvanted HPV-16/18 vaccine in Chinese girls aged 9-17 years: Results from an 8-9-year follow-up phase III open-label study. Asia Pac. J. Clin. Oncol. 2020;16:392–399. doi: 10.1111/ajco.13398.
    1. Naud P.S., Roteli-Martins C.M., De Carvalho N.S., Teixeira J.C., de Borba P.C., Sanchez N., Zahaf T., Catteau G., Geeraerts B., Descamps D. 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. Hum. Vaccines Immunother. 2014;10:2147–2162. doi: 10.4161/hv.29532.
    1. Einstein M.H., Takacs P., Chatterjee A., Sperling R.S., Chakhtoura N., Blatter M.M., Lalezari J., David M.P., 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. Vaccines Immunother. 2014;10:3435–3445. doi: 10.4161/hv.36121.
    1. Huh W.K., Joura E.A., Giuliano A.R., Iversen O.E., de Andrade R.P., Ault K.A., Bartholomew D., Cestero R.M., Fedrizzi E.N., Hirschberg A.L., et al. Final efficacy, immunogenicity, and safety analyses of a nine-valent human papillomavirus vaccine in women aged 16-26 years: A randomised, double-blind trial. Lancet. 2017;390:2143–2159. doi: 10.1016/S0140-6736(17)31821-4.
    1. Toh Z.Q., Kosasih J., Russell F.M., Garland S.M., Mulholland E.K., Licciardi P.V. Recombinant human papillomavirus nonavalent vaccine in the prevention of cancers caused by human papillomavirus. Infect. Drug Resist. 2019;12:1951–1967. doi: 10.2147/IDR.S178381.
    1. Signorelli C., Odone A., Ciorba V., Cella P., Audisio R.A., Lombardi A., Mariani L., Mennini F.S., Pecorelli S., Rezza G., et al. Human papillomavirus 9-valent vaccine for cancer prevention: A systematic review of the available evidence. Epidemiol. Infect. 2017;145:1962–1982. doi: 10.1017/S0950268817000747.
    1. Garland S.M., Kjaer S.K., Muñoz N., Block S.L., Brown D.R., DiNubile M.J., Lindsay B.R., Kuter B.J., Perez G., Dominiak-Felden G., et al. Impact and Effectiveness of the Quadrivalent Human Papillomavirus Vaccine: A Systematic Review of 10 Years of Real-world Experience. Clin. Infect. Dis. 2016;63:519–527. doi: 10.1093/cid/ciw354.
    1. Paavonen J., Naud P., Salmerón J., Wheeler C.M., Chow S.N., Apter D., Kitchener H., Castellsague X., Teixeira J.C., Skinner S.R., 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;374:301–314. doi: 10.1016/S0140-6736(09)61248-4.
    1. Kudo R., Yamaguchi M., Sekine M., Adachi S., Ueda Y., Miyagi E., Hara M., Hanley S.J.B., Enomoto T. Bivalent Human Papillomavirus Vaccine Effectiveness in a Japanese Population: High Vaccine-Type-Specific Effectiveness and Evidence of Cross-Protection. J. Infect. Dis. 2019;219:382–390. doi: 10.1093/infdis/jiy516.
    1. Bogaards J.A., van der Weele P., Woestenberg P.J., van Benthem B.H.B., King A.J. Bivalent Human Papillomavirus (HPV) Vaccine Effectiveness Correlates With Phylogenetic Distance From HPV Vaccine Types 16 and 18. J. Infect. Dis. 2019;220:1141–1146. doi: 10.1093/infdis/jiz280.
    1. Donken R., King A.J., Bogaards J.A., Woestenberg P.J., Meijer C., de Melker H.E. 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;217:1579–1589. doi: 10.1093/infdis/jiy067.
    1. Porras C., Tsang S.H., Herrero R., Guillén D., Darragh T.M., Stoler M.H., Hildesheim A., Wagner S., Boland J., Lowy D.R., et al. Efficacy of the bivalent HPV vaccine against HPV 16/18-associated precancer: Long-term follow-up results from the Costa Rica Vaccine Trial. Lancet Oncol. 2020;21:1643–1652. doi: 10.1016/S1470-2045(20)30524-6.
    1. Garland S.M., Hernandez-Avila M., Wheeler C.M., Perez G., Harper D.M., Leodolter S., Tang G.W., Ferris D.G., Steben M., Bryan J., et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N. Engl. J. Med. 2007;356:1928–1943. doi: 10.1056/NEJMoa061760.
    1. Garland S.M., Pitisuttithum P., Ngan H.Y.S., Cho C.H., Lee C.Y., Chen C.A., Yang Y.C., Chu T.Y., Twu N.F., Samakoses R., et al. Efficacy, Immunogenicity, and Safety of a 9-Valent Human Papillomavirus Vaccine: Subgroup Analysis of Participants From Asian Countries. J. Infect. Dis. 2018;218:95–108. doi: 10.1093/infdis/jiy133.
    1. Ruiz-Sternberg Á.M., Moreira E.D., Jr., Restrepo J.A., Lazcano-Ponce E., Cabello R., Silva A., Andrade R., Revollo F., Uscanga S., Victoria A., et al. Efficacy, immunogenicity, and safety of a 9-valent human papillomavirus vaccine in Latin American girls, boys, and young women. Papillomavirus Res. 2018;5:63–74. doi: 10.1016/j.pvr.2017.12.004.
    1. Joura E.A., Giuliano A.R., Iversen O.E., Bouchard C., Mao C., Mehlsen J., Moreira E.D., Jr., Ngan Y., Petersen L.K., Lazcano-Ponce E., et al. A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N. Engl. J. Med. 2015;372:711–723. doi: 10.1056/NEJMoa1405044.
    1. Malagón T., Drolet M., Boily M.C., Franco E.L., Jit M., Brisson J., Brisson M. Cross-protective efficacy of two human papillomavirus vaccines: A systematic review and meta-analysis. Lancet Infect. Dis. 2012;12:781–789. doi: 10.1016/S1473-3099(12)70187-1.
    1. Lukács A., Máté Z., Farkas N., Mikó A., Tenk J., Hegyi P., Németh B., Czumbel L.M., Wuttapon S., Kiss I., et al. The quadrivalent HPV vaccine is protective against genital warts: A meta-analysis. BMC Public Health. 2020;20:691. doi: 10.1186/s12889-020-08753-y.
    1. Zhang X., Zeng Q., Cai W., Ruan W. Trends of cervical cancer at global, regional, and national level: Data from the Global Burden of Disease study 2019. BMC Public Health. 2021;21:894. doi: 10.1186/s12889-021-10907-5.
    1. Rosenblum H.G., Lewis R.M., Gargano J.W., Querec T.D., Unger E.R., Markowitz L.E. Declines in Prevalence of Human Papillomavirus Vaccine-Type Infection Among Females after Introduction of Vaccine—United States, 2003–2018. MMWR Morb. Mortal. Wkly. Rep. 2021;70:415–420. doi: 10.15585/mmwr.mm7012a2.
    1. Safaeian M., Sampson J.N., Pan Y., Porras C., Kemp T.J., Herrero R., Quint W., van Doorn L.J., Schussler J., Lowy D.R., et al. Durability of Protection Afforded by Fewer Doses of the HPV16/18 Vaccine: The CVT Trial. J. Natl. Cancer Inst. 2018;110:205–212. doi: 10.1093/jnci/djx158.
    1. Zizza A., Banchelli F., Guido M., Marotta C., Di Gennaro F., Mazzucco W., Pistotti V., D’Amico R. Efficacy and safety of human papillomavirus vaccination in HIV-infected patients: A systematic review and meta-analysis. Sci. Rep. 2021;11:4954. doi: 10.1038/s41598-021-83727-7.
    1. Castellsagué X., Muñoz N., Pitisuttithum P., Ferris D., Monsonego J., Ault K., Luna J., Myers E., Mallary S., Bautista O.M., et al. End-of-study safety, immunogenicity, and efficacy of quadrivalent HPV (types 6, 11, 16, 18) recombinant vaccine in adult women 24-45 years of age. Br. J. Cancer. 2011;105:28–37. doi: 10.1038/bjc.2011.185.
    1. Quadrivalent Vaccine against Human Papillomavirus to Prevent High-Grade Cervical Lesions. N. Engl. J. Med. 2007;356:1915–1927. doi: 10.1056/NEJMoa061741.
    1. Muñoz N., Manalastas R., Jr., Pitisuttithum P., Tresukosol D., Monsonego J., Ault K., Clavel C., Luna J., Myers E., Hood S., 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;373:1949–1957. doi: 10.1016/S0140-6736(09)60691-7.
    1. Dobson S.R., McNeil S., Dionne M., Dawar M., Ogilvie G., Krajden M., Sauvageau C., Scheifele D.W., Kollmann T.R., Halperin S.A., et al. Immunogenicity of 2 doses of HPV vaccine in younger adolescents vs 3 doses in young women: A randomized clinical trial. JAMA. 2013;309:1793–1802. doi: 10.1001/jama.2013.1625.
    1. McCormack P.L., Joura E.A. 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;25:339–343. doi: 10.2165/11205060-000000000-00000.
    1. Steinau M., Unger E.R., Hernandez B.Y., Goodman M.T., Copeland G., Hopenhayn C., Cozen W., Saber M.S., Huang Y., Peters E.S., et al. Human papillomavirus prevalence in invasive anal cancers in the United States before vaccine introduction. J. Low. Genit. Tract Dis. 2013;17:397–403. doi: 10.1097/LGT.0b013e31827ed372.
    1. Canadian Immunization C. Summary of Canadian Immunization Committee (CIC) Recommendations for Human Papillomavirus Immunization Programs. Can. Commun. Dis. Rep. 2014;40:152–153. doi: 10.14745/ccdr.v40i08a02.
    1. Block S.L., Nolan T., Sattler C., Barr E., Giacoletti K.E., Marchant C.D., Castellsagué X., Rusche S.A., Lukac S., Bryan J.T., 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;118:2135–2145. doi: 10.1542/peds.2006-0461.
    1. Giuliano A.R., Palefsky J.M., Goldstone S., Moreira E.D., Jr., Penny M.E., Aranda C., Vardas E., Moi H., Jessen H., Hillman R., et al. Efficacy of quadrivalent HPV vaccine against HPV Infection and disease in males. N. Engl. J. Med. 2011;364:401–411. doi: 10.1056/NEJMoa0909537.
    1. Palefsky J.M., Giuliano A.R., Goldstone S., Moreira E.D., Jr., Aranda C., Jessen H., Hillman R., Ferris D., Coutlee F., Stoler M.H., et al. HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. N. Engl. J. Med. 2011;365:1576–1585. doi: 10.1056/NEJMoa1010971.
    1. Spinner C., Ding L., Bernstein D.I., Brown D.R., Franco E.L., Covert C., Kahn J.A. Human Papillomavirus Vaccine Effectiveness and Herd Protection in Young Women. Pediatrics. 2019;143:e20181902. doi: 10.1542/peds.2018-1902.
    1. Baandrup L., Blomberg M., Dehlendorff C., Sand C., Andersen K.K., Kjaer S.K. Significant decrease in the incidence of genital warts in young Danish women after implementation of a national human papillomavirus vaccination program. Sex. Transm. Dis. 2013;40:130–135. doi: 10.1097/OLQ.0b013e31827bd66b.
    1. Chow E.P., Read T.R., Wigan R., Donovan B., Chen M.Y., Bradshaw C.S., Fairley C.K. Ongoing decline in genital warts among young heterosexuals 7 years after the Australian human papillomavirus (HPV) vaccination programme. Sex. Transm. Infect. 2015;91:214–219. doi: 10.1136/sextrans-2014-051813.
    1. Herweijer E., Sundström K., Ploner A., Uhnoo I., Sparén P., Arnheim-Dahlström L. Quadrivalent HPV vaccine effectiveness against high-grade cervical lesions by age at vaccination: A population-based study. Int. J. Cancer. 2016;138:2867–2874. doi: 10.1002/ijc.30035.
    1. Baldur-Felskov B., Dehlendorff C., Junge J., Munk C., Kjaer S.K. Incidence of cervical lesions in Danish women before and after implementation of a national HPV vaccination program. Cancer Causes Control. 2014;25:915–922. doi: 10.1007/s10552-014-0392-4.
    1. Baldur-Felskov B., Dehlendorff C., Munk C., Kjaer S.K. Early impact of human papillomavirus vaccination on cervical neoplasia--nationwide follow-up of young Danish women. J. Natl. Cancer Inst. 2014;106:djt460. doi: 10.1093/jnci/djt460.
    1. Brotherton J.M.L., Malloy M., Budd A.C., Saville M., Drennan K.T., Gertig D.M. 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. doi: 10.1016/j.pvr.2015.05.005.
    1. Markowitz L.E., Hariri S., Lin C., Dunne E.F., Steinau M., McQuillan G., Unger E.R. Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003–2010. J. Infect. Dis. 2013;208:385–393. doi: 10.1093/infdis/jit192.
    1. Mix J.M., Van Dyne E.A., Saraiya M., Hallowell B.D., Thomas C.C. Assessing Impact of HPV Vaccination on Cervical Cancer Incidence among Women Aged 15-29 Years in the United States, 1999-2017: An Ecologic Study. Cancer Epidemiol. Biomark. Prev. 2021;30:30–37. doi: 10.1158/1055-9965.EPI-20-0846.
    1. Oliver S.E., Unger E.R., Lewis R., McDaniel D., Gargano J.W., Steinau M., Markowitz L.E. Prevalence of Human Papillomavirus Among Females After Vaccine Introduction-National Health and Nutrition Examination Survey, United States, 2003–2014. J. Infect. Dis. 2017;216:594–603. doi: 10.1093/infdis/jix244.
    1. Safaeian M., Porras C., Pan Y., Kreimer A., Schiller J.T., Gonzalez P., Lowy D.R., Wacholder S., Schiffman M., Rodriguez A.C., et al. Durable antibody responses following one dose of the bivalent human papillomavirus L1 virus-like particle vaccine in the Costa Rica Vaccine Trial. Cancer Prev. Res. 2013;6:1242–1250. doi: 10.1158/1940-6207.CAPR-13-0203.
    1. Kreimer A.R., Sampson J.N., Porras C., Schiller J.T., Kemp T., Herrero R., Wagner S., Boland J., Schussler J., Lowy D.R., et al. Evaluation of Durability of a Single Dose of the Bivalent HPV Vaccine: The CVT Trial. J. Natl. Cancer Inst. 2020;112:1038–1046. doi: 10.1093/jnci/djaa011.
    1. Verdoodt F., Dehlendorff C., Kjaer S.K. Dose-related Effectiveness of Quadrivalent Human Papillomavirus Vaccine Against Cervical Intraepithelial Neoplasia: A Danish Nationwide Cohort Study. Clin. Infect. Dis. 2020;70:608–614. doi: 10.1093/cid/ciz239.
    1. van Aar F., Mooij S.H., van der Sande M.A.B., Speksnijder A.G.C.L., Stolte I.G., Meijer C.J.L.M., Verhagen D.W.M., King A.J., de Vries H.J.C., van der Loeff M.F.S. Anal and penile high-risk human papillomavirus prevalence in HIV-negative and HIV-infected MSM. AIDS. 2013;27:2921–2931. doi: 10.1097/01.aids.0000432541.67409.3c.
    1. Zhou Y., Lin Y.F., Gao L., Dai J., Luo G., Li L., Yuan T., Li P., Zhan Y., Gao Y., et al. Human papillomavirus prevalence among men who have sex with men in China: A systematic review and meta-analysis. Eur. J. Clin. Microbiol. Infect. Dis. 2021;40:1357–1367. doi: 10.1007/s10096-021-04229-y.
    1. Wei F., Gaisa M.M., D’Souza G., Xia N., Giuliano A.R., Hawes S.E., Gao L., Cheng S.H., Donà M.G., Goldstone S.E., et al. Epidemiology of anal human papillomavirus infection and high-grade squamous intraepithelial lesions in 29 900 men according to HIV status, sexuality, and age: A collaborative pooled analysis of 64 studies. Lancet HIV. 2021;8:e531–e543. doi: 10.1016/S2352-3018(21)00108-9.
    1. Mooij S.H., Boot H.J., Speksnijder A.G., Stolte I.G., Meijer C.J., Snijders P.J., Verhagen D.W., King A.J., de Vries H.J., Quint W.G., et al. Oral human papillomavirus infection in HIV-negative and HIV-infected MSM. Aids. 2013;27:2117–2128. doi: 10.1097/QAD.0b013e328362395c.
    1. King E.M., Oomeer S., Gilson R., Copas A., Beddows S., Soldan K., Jit M., Edmunds W.J., Sonnenberg P. Oral Human Papillomavirus Infection in Men Who Have Sex with Men: A Systematic Review and Meta-Analysis. PLoS ONE. 2016;11:e0157976. doi: 10.1371/journal.pone.0157976.
    1. Edelstein Z.R., Carter J.J., Garg R., Winer R.L., Feng Q., Galloway D.A., Koutsky L.A. Serum antibody response following genital {alpha}9 human papillomavirus infection in young men. J. Infect. Dis. 2011;204:209–216. doi: 10.1093/infdis/jir242.
    1. Drolet M., Bénard É., Boily M.C., Ali H., Baandrup L., Bauer H., Beddows S., Brisson J., Brotherton J.M., Cummings T., et al. Population-level impact and herd effects following human papillomavirus vaccination programmes: A systematic review and meta-analysis. Lancet Infect. Dis. 2015;15:565–580. doi: 10.1016/S1473-3099(14)71073-4.
    1. Swedish K.A., Goldstone S.E. Prevention of anal condyloma with quadrivalent human papillomavirus vaccination of older men who have sex with men. PLoS ONE. 2014;9:e93393. doi: 10.1371/journal.pone.0093393.
    1. Swedish K.A., Factor S.H., Goldstone S.E. Prevention of recurrent high-grade anal neoplasia with quadrivalent human papillomavirus vaccination of men who have sex with men: A nonconcurrent cohort study. Clin. Infect. Dis. 2012;54:891–898. doi: 10.1093/cid/cir1036.
    1. Hillman R.J., Giuliano A.R., Palefsky J.M., Goldstone S., Moreira E.D., Jr., Vardas E., Aranda C., Jessen H., Ferris D.G., Coutlee F., et al. Immunogenicity of the quadrivalent human papillomavirus (type 6/11/16/18) vaccine in males 16 to 26 years old. Clin. Vaccine Immunol. 2012;19:261–267. doi: 10.1128/CVI.05208-11.
    1. Castellsagué X., Giuliano A.R., Goldstone S., Guevara A., Mogensen O., Palefsky J.M., Group T., Shields C., Liu K., Maansson R., et al. Immunogenicity and safety of the 9-valent HPV vaccine in men. Vaccine. 2015;33:6892–6901. doi: 10.1016/j.vaccine.2015.06.088.
    1. Public Health England (PHE): Producing Estimates of the Size of the LGB Population of England. [(accessed on 10 November 2021)]; Available online: .
    1. You E.L., Henry M., Zeitouni A.G. Human papillomavirus-associated oropharyngeal cancer: Review of current evidence and management. Curr. Oncol. 2019;26:119–123. doi: 10.3747/co.26.4819.
    1. Diana G., Corica C. Human Papilloma Virus vaccine and prevention of head and neck cancer, what is the current evidence? Oral Oncol. 2021;115:105168. doi: 10.1016/j.oraloncology.2020.105168.
    1. Pinto L.A., Kemp T.J., Torres B.N., Isaacs-Soriano K., Ingles D., Abrahamsen M., Pan Y., Lazcano-Ponce E., Salmeron J., Giuliano A.R. Quadrivalent Human Papillomavirus (HPV) Vaccine Induces HPV-Specific Antibodies in the Oral Cavity: Results From the Mid-Adult Male Vaccine Trial. J. Infect. Dis. 2016;214:1276–1283. doi: 10.1093/infdis/jiw359.
    1. Lehtinen M., Apter D., Eriksson T., Harjula K., Hokkanen M., Lehtinen T., Natunen K., Damaso S., Soila M., Bi D., et al. Effectiveness of the AS04-adjuvanted HPV-16/18 vaccine in reducing oropharyngeal HPV infections in young females-Results from a community-randomized trial. Int. J. Cancer. 2020;147:170–174. doi: 10.1002/ijc.32791.
    1. Chaturvedi A.K., Graubard B.I., Broutian T., Pickard R.K.L., Tong Z.-Y., Xiao W., Kahle L., Gillison M.L. Effect of Prophylactic Human Papillomavirus (HPV) Vaccination on Oral HPV Infections Among Young Adults in the United States. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2018;36:262–267. doi: 10.1200/JCO.2017.75.0141.
    1. Hirth J.M., Chang M., Resto V.A. Prevalence of oral human papillomavirus by vaccination status among young adults (18–30 years old) Vaccine. 2017;35:3446–3451. doi: 10.1016/j.vaccine.2017.05.025.
    1. Lin C., Franceschi S., Clifford G.M. Human papillomavirus types from infection to cancer in the anus, according to sex and HIV status: A systematic review and meta-analysis. Lancet Infect. Dis. 2018;18:198–206. doi: 10.1016/S1473-3099(17)30653-9.
    1. Bruggink S.C., de Koning M.N., Gussekloo J., Egberts P.F., Ter Schegget J., Feltkamp M.C., Bavinck J.N., Quint W.G., Assendelft W.J., Eekhof J.A. Cutaneous wart-associated HPV types: Prevalence and relation with patient characteristics. J. Clin. Virol. 2012;55:250–255. doi: 10.1016/j.jcv.2012.07.014.
    1. Patel A.S., Karagas M.R., Perry A.E., Nelson H.H. Exposure profiles and human papillomavirus infection in skin cancer: An analysis of 25 genus beta-types in a population-based study. J. Investig. Derm. 2008;128:2888–2893. doi: 10.1038/jid.2008.162.
    1. Iannacone M.R., Gheit T., Waterboer T., Giuliano A.R., Messina J.L., Fenske N.A., Cherpelis B.S., Sondak V.K., Roetzheim R.G., Ferrer-Gil S., et al. Case-control study of cutaneous human papillomavirus infection in Basal cell carcinoma of the skin. J. Investig. Derm. 2013;133:1512–1520. doi: 10.1038/jid.2012.478.
    1. Iannacone M.R., Gheit T., Pfister H., Giuliano A.R., Messina J.L., Fenske N.A., Cherpelis B.S., Sondak V.K., Roetzheim R.G., Silling S., et al. Case-control study of genus-beta human papillomaviruses in plucked eyebrow hairs and cutaneous squamous cell carcinoma. Int. J. Cancer. 2014;134:2231–2244. doi: 10.1002/ijc.28552.
    1. Struijk L., Hall L., van der Meijden E., Wanningen P., Bavinck J.N., Neale R., Green A.C., Ter Schegget J., Feltkamp M.C. Markers of cutaneous human papillomavirus infection in individuals with tumor-free skin, actinic keratoses, and squamous cell carcinoma. Cancer Epidemiol. Biomark. Prev. 2006;15:529–535. doi: 10.1158/1055-9965.EPI-05-0747.
    1. Bouwes Bavinck J.N., Stark S., Petridis A.K., Marugg M.E., Ter Schegget J., Westendorp R.G., Fuchs P.G., Vermeer B.J., Pfister H. The presence of antibodies against virus-like particles of epidermodysplasia verruciformis-associated humanpapillomavirus type 8 in patients with actinic keratoses. Br. J. Derm. 2000;142:103–109. doi: 10.1046/j.1365-2133.2000.03248.x.
    1. Harwood C.A., Surentheran T., McGregor J.M., Spink P.J., Leigh I.M., Breuer J., Proby C.M. Human papillomavirus infection and non-melanoma skin cancer in immunosuppressed and immunocompetent individuals. J. Med. Virol. 2000;61:289–297. doi: 10.1002/1096-9071(200007)61:3<289::AID-JMV2>;2-Z.
    1. Vinzón S.E., Braspenning-Wesch I., Müller M., Geissler E.K., Nindl I., Gröne H.-J., Schäfer K., Rösl F. Protective vaccination against papillomavirus-induced skin tumors under immunocompetent and immunosuppressive conditions: A preclinical study using a natural outbred animal model. PLoS Pathog. 2014;10:e1003924. doi: 10.1371/journal.ppat.1003924.
    1. Vinzón S.E., Rösl F. HPV vaccination for prevention of skin cancer. Hum. Vaccines Immunother. 2015;11:353–357. doi: 10.4161/21645515.2014.983858.
    1. Alphs H.H., Gambhira R., Karanam B., Roberts J.N., Jagu S., Schiller J.T., Zeng W., Jackson D.C., Roden R.B. Protection against heterologous human papillomavirus challenge by a synthetic lipopeptide vaccine containing a broadly cross-neutralizing epitope of L2. Proc. Natl. Acad. Sci. USA. 2008;105:5850–5855. doi: 10.1073/pnas.0800868105.
    1. Schellenbacher C., Kwak K., Fink D., Shafti-Keramat S., Huber B., Jindra C., Faust H., Dillner J., Roden R.B.S., Kirnbauer R. Efficacy of RG1-VLP vaccination against infections with genital and cutaneous human papillomaviruses. J. Investig. Derm. 2013;133:2706–2713. doi: 10.1038/jid.2013.253.
    1. Vermaelen K. Vaccine Strategies to Improve Anti-cancer Cellular Immune Responses. Front. Immunol. 2019;10:8. doi: 10.3389/fimmu.2019.00008.
    1. Yeo-Teh N.S.L., Ito Y., Jha S. High-Risk Human Papillomaviral Oncogenes E6 and E7 Target Key Cellular Pathways to Achieve Oncogenesis. Int. J. Mol. Sci. 2018;19:1706. doi: 10.3390/ijms19061706.
    1. Araldi R.P., Sant’Ana T.A., Módolo D.G., de Melo T.C., Spadacci-Morena D.D., de Cassia Stocco R., Cerutti J.M., de Souza E.B. The human papillomavirus (HPV)-related cancer biology: An overview. Biomed. Pharm. 2018;106:1537–1556. doi: 10.1016/j.biopha.2018.06.149.
    1. Ikeda Y., Uemura Y., Asai-Sato M., Nakao T., Nakajima T., Iwata T., Akiyama A., Satoh T., Yahata H., Kato K., et al. Safety and efficacy of mucosal immunotherapy using human papillomavirus (HPV) type 16 E7-expressing Lactobacillus-based vaccine for the treatment of high-grade squamous intraepithelial lesion (HSIL): The study protocol of a randomized placebo-controlled clinical trial (MILACLE study) Jpn. J. Clin. Oncol. 2019;49:877–880. doi: 10.1093/jjco/hyz095.
    1. Bhuyan P.K., Dallas M., Kraynyak K., Herring T., Morrow M., Boyer J., Duff S., Kim J., Weiner D.B. Durability of response to VGX-3100 treatment of HPV16/18 positive cervical HSIL. Hum. Vaccines Immunother. 2021;17:1288–1293. doi: 10.1080/21645515.2020.1823778.
    1. Dorta-Estremera S., Chin R.L., Sierra G., Nicholas C., Yanamandra A.V., Nookala S.M.K., Yang G., Singh S., Curran M.A., Sastry K.J. Mucosal HPV E6/E7 Peptide Vaccination in Combination with Immune Checkpoint Modulation Induces Regression of HPV(+) Oral Cancers. Cancer Res. 2018;78:5327–5339. doi: 10.1158/0008-5472.CAN-18-0892.
    1. Vvax001 Cancer Vaccine in (Pre) Malignant Cervical Lesions. Identifier NCT03141463. [(accessed on 15 November 2021)]; Available online: .
    1. Chu N.R., Wu H.B., Wu T.C., Boux L.J., Mizzen L.A., Siegel M.I. Immunotherapy of a human papillomavirus type 16 E7-expressing tumor by administration of fusion protein comprised of Mycobacterium bovis BCG Hsp65 and HPV16 E7. Cell Stress Chaperones. 2000;5:401–405. doi: 10.1379/1466-1268(2000)005<0401:IOAHPT>;2.
    1. Taylor S., Ryser M., Mihalyi A., van Effelterre T. Response letter regarding the letter to the editors by Brown et al. Hum. Vaccines Immunother. 2016;12:1943–1946. doi: 10.1080/21645515.2016.1151598.
    1. Gardasil 9. [(accessed on 23 October 2021)]; Available online: .
    1. Gardasil. [(accessed on 23 October 2021)]; Available online: .

Source: PubMed

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