The predicted impact of vaccination on human papillomavirus infections in Australia
Megan A. Smith
Cancer Epidemiology Research Unit, The Cancer Council New South Wales, Woolloomooloo, New South Wales, Australia
Search for more papers by this authorCorresponding Author
Karen Canfell
Cancer Epidemiology Research Unit, The Cancer Council New South Wales, Woolloomooloo, New South Wales, Australia
Fax: +61-2-93341778
Cancer Epidemiology Research Unit, The Cancer Council NSW, 153 Dowling Street, Woolloomooloo, NSW, AustraliaSearch for more papers by this authorJulia M.L. Brotherton
National Centre for Immunisation Research and Surveillance, The Children's Hospital at Westmead, Westmead, New South Wales, Australia
Search for more papers by this authorJie-Bin Lew
Cancer Epidemiology Research Unit, The Cancer Council New South Wales, Woolloomooloo, New South Wales, Australia
Search for more papers by this authorRuanne V. Barnabas
HIV Vaccine Trials Network, Fred Hutchinson Cancer Research Center, Seattle, WA
Search for more papers by this authorMegan A. Smith
Cancer Epidemiology Research Unit, The Cancer Council New South Wales, Woolloomooloo, New South Wales, Australia
Search for more papers by this authorCorresponding Author
Karen Canfell
Cancer Epidemiology Research Unit, The Cancer Council New South Wales, Woolloomooloo, New South Wales, Australia
Fax: +61-2-93341778
Cancer Epidemiology Research Unit, The Cancer Council NSW, 153 Dowling Street, Woolloomooloo, NSW, AustraliaSearch for more papers by this authorJulia M.L. Brotherton
National Centre for Immunisation Research and Surveillance, The Children's Hospital at Westmead, Westmead, New South Wales, Australia
Search for more papers by this authorJie-Bin Lew
Cancer Epidemiology Research Unit, The Cancer Council New South Wales, Woolloomooloo, New South Wales, Australia
Search for more papers by this authorRuanne V. Barnabas
HIV Vaccine Trials Network, Fred Hutchinson Cancer Research Center, Seattle, WA
Search for more papers by this authorAbstract
Vaccines based on human papillomavirus (HPV) 16 and 18 virus-like particles have the potential to prevent ∼70% of cervical cancers. In Australia, public vaccination against HPV commenced in April 2007, and includes routine vaccination of females aged 12–13 years, and a 2-year school and GP-based catch-up in females aged 12–26 years. The objectives of this study were to estimate initial vaccination coverage rates, to describe current patterns of sexual behavior in young females, and to predict the impact of vaccination on HPV16 infections. We reviewed early coverage data, estimating that coverage in 2007/2008 will reach 86% (feasible range 67–90%) for 12- to 13-year-old girls, with lower rates attained in older females. A review of survey data found that the median age of first intercourse in Australian females is 16 years, with ∼90% of women sexually active at 22 years. Using these data, we performed an analysis of HPV transmission to predict the impact of vaccination on HPV infection rates. The public program is predicted to result in a reduction in the age-standardized incidence of HPV16 infections of 56% by 2010 (feasible range 48–61%), and 92% by 2050 (feasible range 76–95%). Elective vaccination of older women and vaccination of males may provide some incremental gains, but the benefits to women of vaccinating males will be less if coverage of females remains high. In conclusion, the current vaccination program is expected to result in a substantial and rapid reduction in the incidence of HPV16 in Australia. © 2008 Wiley-Liss, Inc.
References
- 1
Walboomers JM,Jacobs MV,Manos MM,Bosch FX,Kummer JA,Shah KV,Snijders PJ,Peto J,Meijer CJ,Munoz N.
Human papillomavirus is a necessary cause of invasive cervical cancer worldwide.
J Pathol
1999;
189:
12–9.
10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F CAS PubMed Web of Science® Google Scholar
- 2 Munoz N,Bosch FX,de Sanjose S,Herrero R,Castellsague X,Shah KV,Snijders PJ,Meijer CJ. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003; 348: 518–27.
- 3 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.
- 4 Villa LL,Costa RL,Petta CA,Andrade RP,Paavonen J,Iversen OE,Olsson SE,Hoye J,Steinwall M,Riis-Johannessen G,Andersson-Ellstrom A,Elfgren K, et al. 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. Br J Cancer 2006; 95: 1459–66.
- 5 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.
- 6 Villa LL,Costa RL,Petta CA,Andrade RP,Ault KA,Giuliano AR,Wheeler CM,Koutsky LA,Malm C,Lehtinen M,Skjeldestad FE,Olsson SE, et al. 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 Oncol 2005; 6: 271–8.
- 7 Harper DM,Franco EL,Wheeler C,Ferris DG,Jenkins D,Schuind A,Zahaf T,Innis B,Naud P,De Carvalho NS,Roteli-Martins CM,Teixeira J, 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.
- 8 Clifford G,Franceschi S,Diaz M,Munoz N,Villa LL. Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases. Vaccine 2006; 24( Suppl 3): S26–S34.
- 9 Stevens MP,Tabrizi SN,Quinn MA,Garland SM. Human papillomavirus genotype prevalence in cervical biopsies from women diagnosed with cervical intraepithelial neoplasia or cervical cancer in Melbourne, Australia. Int J Gynecol Cancer 2006; 16: 1017–24.
- 10 Commonwealth of Australia Gazette, No. GN 25, 28 June 2006. [Internet] 2007 [cited 25 June 2007]. Available from: http://www.tga.gov.au/docs/html/adec/adec0246.htm.
- 11 Australian Bureau of Statistics. 4221.0 Schools, Australia, 2006. Australia: Australian Bureau of Statistics, Available from: http://www.abs.gov.au/AUSSTATS/[email protected]/DetailsPage/4221.02006?Open Document.
- 12 Australian Government. State/Territory HPV Vaccination Program Schedule. [cited 25 June 2007] Available from: http://www.health.gov.au/internet/standby/publishing.nsf/Content/state-territory-hpv-vac-sched/$file/state-territory-hpv-vac-sched.pdf.
- 13 GlaxoSmithKline. Another Australia first in the fight against cervical cancer: new vaccine for women 27–45 years, Press Release, 14 August 2007. Available from: http://www.gsk.com.au/media-centre_detail.aspx?view=220.
- 14 Skinner SR,Nolan T,Bowes G. Measles-mumps-rubella and hepatitis B vaccination uptake in adolescents: a survey in metropolitan Melbourne. Med J Aust 1998; 168: 546–9.
- 15 Skinner SR,Imberger A,Nolan T,Lester R,Glover S,Bowes G. Randomised controlled trial of an educational strategy to increase school-based adolescent hepatitis B vaccination. Aust N Z J Public Health 2000; 24: 298–304.
- 16 State and territory Public Health Outcome Funding Agreements 2000/2001 and 2001/2002. Department of Health and Ageing, Australian Government 2006 March 2007. [Internet] 2007. [cited 1 May 2007]. Available from: http://www.health.gov.au/internet/wcms/publishing.nsf/Content/health-pubhlth-about-phofa-phofa.htm.
- 17 Heron L,O'Connor B,Chant K,Jalaludin B. A cluster randomised trial of three hepatitis B vaccination programs targeting children in late primary school. [abstract] Communicable Diseases Control Conference 31 March–1 April 2003, Canberra 2003, p 51.
- 18 Bowden FJ,O'Keefe EJ,Primrose R,Currie MJ. Sexually transmitted infections, blood-borne viruses and risk behaviour in an Australian senior high school population—the SHLiRP study. Sex Health 2005; 2: 229–36.
- 19 de Visser R,Smith A,Richters J. Can we generalise to other young people from studies of sexual risk behaviour among university students? Aust N Z J Public Health 2005; 29: 436–41.
- 20 Dunne MP,Donald M,Lucke J,Nilsson R,Ballard R,Raphael B. Age-related increase in sexual behaviours and decrease in regular condom use among adolescents in Australia. Int J STD AIDS 1994; 5: 41–7.
- 21 Estcourt CS,Marks C,Rohrsheim R,Johnson AM,Donovan B,Mindel A. HIV, sexually transmitted infections, and risk behaviours in male commercial sex workers in Sydney. Sex Transm Infect 2000; 76: 294–8.
- 22 Holden CA,McLachlan RI,Cumming R,Wittert G,Handelsman DJ,de Kretser DM,Pitts M. Sexual activity, fertility and contraceptive use in middle-aged and older men: Men in Australia, Telephone Survey (MATeS). Hum Reprod 2005; 20: 3429–34.
- 23 Kang MS,Zador DA. Sexual behaviour and contraceptive practices of year 10 schoolgirls in inner metropolitan Sydney. Aust J Marriage Fam 1993; 14: 137–42.
- 24 Pyett PM,Haste BR,Snow JD. Who works in the sex industry? A profile of female prostitutes in Victoria. Aust N Z J Public Health 1996; 20: 431–3.
- 25 Smith AM,Rissel CE,Richters J,Grulich AE,de Visser RO. Sex in Australia: reflections and recommendations for future research. Aust N Z J Public Health 2003; 27: 251–6.
- 26 Rosenthal D,Fernbach M,Moore S. The singles scene: safe sex practices and attitudes among at-risk heterosexual adults. Psychol Health 1997; 12: 171–82.
- 27 Smith A,Agius P,Dyson S,Mitchell A,Pitts M. Secondary students and sexual health 2002. Melbourne: Australian Research Centre in Sex, Health and Society, La Trobe University, 2003.
- 28 The Australian National University. The Australian Social Science Data Archive. [Internet] 2006 [cited 4 August 2006]. Available from: http://assda.anu.edu.au/index.html.
- 29 Weisberg E,North P,Buxton M. Sexual activity and condom use in high school students. Med J Aust 1992; 156: 612–13.
- 30 Rosenthal DA,Smith AM,de Visser R. Personal and social factors influencing age at first sexual intercourse. Arch Sex Behav 1999; 28: 319–33.
- 31 Grunseit AC,Richters J. Age at first intercourse in an Australian national sample of technical college students. Aust N Z J Public Health 2000; 24: 11–16.
- 32 Garnett GP,Anderson RM. Factors controlling the spread of HIV in heterosexual communities in developing countries: patterns of mixing between different age and sexual activity classes. Philos Trans R Soc Lond B Biol Sci 1993; 342: 137–59.
- 33 Barnabas RV,Laukkanen P,Koskela P,Kontula O,Lehtinen M,Garnett GP. Epidemiology of HPV 16 and cervical cancer in Finland and the potential impact of vaccination: mathematical modelling analyses. PLoS Med 2006; 3: e138.
- 34 Myers ER,McCrory DC,Nanda K,Bastian L,Matchar DB. Mathematical model for the natural history of human papillomavirus infection and cervical carcinogenesis. Am J Epidemiol 2000; 151: 1158–71.
- 35 Canfell K,Barnabas R,Patnick J,Beral V. The predicted effect of changes in cervical screening practice in the UK: results from a modelling study. Br J Cancer 2004; 91: 530–6.
- 36 Schiffman M. Integration of human papillomavirus vaccination, cytology, and human papillomavirus testing. Cancer 2007; 111: 145–53.
- 37 Carter JJ,Koutsky LA,Hughes JP,Lee SK,Kuypers J,Kiviat N,Galloway DA. Comparison of human papillomavirus types 16, 18, and 6 capsid antibody responses following incident infection. J Infect Dis 2000; 181: 1911–9.
- 38 Frazer I. Vaccines for papillomavirus infection. Virus Res 2002; 89: 271–4.
- 39 de Gruijl TD,Bontkes HJ,Walboomers JM,Schiller JT,Stukart MJ,Groot BS,Chabaud MM,Remmink AJ,Verheijen RH,Helmerhorst TJ,Meijer CJ,Scheper RJ. Immunoglobulin G responses against human papillomavirus type 16 virus-like particles in a prospective nonintervention cohort study of women with cervical intraepithelial neoplasia. J Natl Cancer Inst 1997; 89: 630–8.
- 40 Wideroff L,Schiffman M,Haderer P,Armstrong A,Greer CE,Manos MM,Burk RD,Scott DR,Sherman ME,Schiller JT,Hoover RN,Tarone RE, et al. Seroreactivity to human papillomavirus types 16, 18, 31, and 45 virus-like particles in a case–control study of cervical squamous intraepithelial lesions. J Infect Dis 1999; 180: 1424–8.
- 41 Moscicki AB,Schiffman M,Kjaer S,Villa LL. Chapter 5: updating the natural history of HPV and anogenital cancer. Vaccine 2006; 24 ( Suppl 3): S42–S51.
- 42 Hughes JP,Garnett GP,Koutsky L. The theoretical population-level impact of a prophylactic human papilloma virus vaccine. Epidemiology 2002; 13: 631–9.
- 43 French KM,Barnabas RV,Lehtinen M,Kontula O,Pukkala E,Dillner J,Garnett GP. Strategies for the introduction of human papillomavirus vaccination: modelling the optimum age- and sex-specific pattern of vaccination in Finland. Br J Cancer 2007; 96: 514–18.
- 44 Elbasha EH,Dasbach EJ,Insinga RP. Model for assessing human papillomavirus vaccination strategies. Emerg Infect Dis 2007; 13: 28–41.
- 45 Goldie SJ,Kohli M,Grima D,Weinstein MC,Wright TC,Bosch FX,Franco E. Projected clinical benefits and cost-effectiveness of a human papillomavirus 16/18 vaccine. J Natl Cancer Inst 2004; 96: 604–15.
- 46 Kulasingam SL,Myers ER. Potential health and economic impact of adding a human papillomavirus vaccine to screening programs. JAMA 2003; 290: 781–9.
- 47 Sanders GD,Taira AV. Cost-effectiveness of a potential vaccine for human papillomavirus. Emerg Infect Dis 2003; 9: 37–48.
- 48 Taira AV,Neukermans CP,Sanders GD. Evaluating human papillomavirus vaccination programs. Emerg Infect Dis 2004; 10: 1915–23.
- 49 Kohli M,Ferko N,Martin A,Franco EL,Jenkins D,Gallivan S,Sherlaw-Johnson C,Drummond M. Estimating the long-term impact of a prophylactic human papillomavirus 16/18 vaccine on the burden of cervical cancer in the UK. Br J Cancer 2007; 96: 143–50.
- 50 van de Velde N,Brisson M,Boily MC. Modeling human papillomavirus vaccine effectiveness: quantifying the impact of parameter uncertainty. Am J Epidemiol 2007; 165: 762–75.
- 51 Garnett GP,Kim JJ,French K,Goldie SJ. Chapter 21: modelling the impact of HPV vaccines on cervical cancer and screening programmes. Vaccine 2006; 24( Suppl 3): S178–S186.
- 52 Regan DG,Philp DJ,Hocking JS,Law MG. Modelling the population-level impact of vaccination on the transmission of human papillomavirus type 16 in Australia. Sex Health 2007; 4: 147–63.
- 53 Reisinger KS,Block SL,Lazcano-Ponce E,Samakoses R,Esser MT,Erick J,Puchalski D,Giacoletti KE,Sings HL,Lukac S,Alvarez FB,Barr E. 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. Pediatr Infect Dis J 2007; 26: 201–9.
- 54 Block SL,Nolan T,Sattler C,Barr E,Giacoletti KE,Marchant CD,Castellsague X,Rusche SA,Lukac S,Bryan JT,Cavanaugh PF,Jr,Reisinger KS. 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.
- 55 McNeil C. Coming soon: cervical cancer vaccines, and an array of public health issues. J Natl Cancer Inst 2006; 98: 432–4.
- 56 Hildesheim A,Herrero R,Wacholder S,Rodriguez AC,Solomon D,Bratti MC,Schiller JT,Gonzalez P,Dubin G,Porras C,Jimenez SE,Lowy DR, et al. Effect of human papillomavirus 16/18 L1 viruslike particle vaccine among young women with preexisting infection: a randomized trial. JAMA 2007; 298: 743–53.
- 57 Olsson SE,Villa LL,Costa RL,Petta CA,Andrade RP,Malm C,Iversen OE,Hoye J,Steinwall M,Riis-Johannessen G,Andersson-Ellstrom A,Elfgren K, et al. Induction of immune memory following administration of a prophylactic quadrivalent human papillomavirus (HPV) types 6/11/16/18 L1 virus-like particle (VLP) vaccine. Vaccine 2007; 25: 4931–9.
- 58 Canfell K,Sitas F,Beral V. Cervical cancer in Australia and the United Kingdom: comparison of screening policy and uptake, and cancer incidence and mortality. Med J Aust 2006; 185: 482–6.
- 59 Garland SM,Brotherton J,Condon J,Tabrizi S,McIntyre P,Smith D,Paul R. Human papillomavirus genotype prevalence in australian women (indigenous, non-indigenous, urban, rural populations). In: Proceedings of the 24th International Papillomavirus Society Conference, Beijing, China, 9 November 2007.
- 60 Burchell AN,Winer RL,de Sanjose S,Franco EL. Chapter 6: Epidemiology and transmission dynamics of genital HPV infection. Vaccine 2006; 24( Suppl 3): S52–S61.
- 61 Commonwealth Department of Health and Aged Care. Let's work together to beat measles: a report on Australia's measles control campaign. Commonwealth Department of Health and Aged Care, 2000.
- 62 Madin S. The rollout of the vaccination program – the Victorian experience. Is this the end of cervical cancer? The impact of vaccination & HPV DNA testing; Melbourne: Asia Oceania Research Organisation on Genital Infections & Neoplasia (AOGIN); 2007.
- 63 McClelland A,Liamputtong P. Knowledge and acceptance of human papillomavirus vaccination: perspectives of young Australians living in Melbourne, Australia. Sex Health 2006; 3: 95–101.
- 64 Marshall H,Ryan P,Roberton D,Baghurst P. A cross-sectional survey to assess community attitudes to introduction of human papillomavirus vaccine. Aust N Z J Public Health 2007; 31: 235–42.
- 65 Pitts MK,Dyson SJ,Rosenthal DA,Garland SM. Knowledge and awareness of human papillomavirus (HPV): attitudes towards HPV vaccination among a representative sample of women in Victoria, Australia. Sex Health 2007; 4: 177–80.
- 66 Australian Institute of Health and Welfare (AIHW). Cervical screening in Australia 2004–2005, AIHW Cat. No. Can 38 ed. Canberra: Australian Institute of Health and Welfare (Cancer Series Number 38), 2007.
- 67 Taylor A,Wilson D,Dal Grande E,Gill T. National Influenza Survey (A population survey of vaccination uptake in Australia). South Australian Department of Human Services Centre for Population Studies in Epidemiology, Epidemiology Branch, 2000.
- 68 Australian Institute of Health and Welfare 2005. 2004 Adult Vaccination Survey: summary results. AIHW cat. no. PHE 56. Canberra: AIHW & DoHA. 2005.
- 69 Rissel CE,Richters J,Grulich AE,de Visser RO,Smith AM. Sex in Australia: first experiences of vaginal intercourse and oral sex among a representative sample of adults. Aust N Z J Public Health 2003; 27: 131–7.
- 70 Boyle FM,Dunne MP,Purdie DM,Najman JM,Cook MD. Early patterns of sexual activity: age cohort differences in Australia. Int J STD AIDS 2003; 14: 745–52.
- 71 de Visser RO,Smith AM,Rissel CE,Richters J,Grulich AE. Sex in Australia: heterosexual experience and recent heterosexual encounters among a representative sample of adults. Aust N Z J Public Health 2003; 27: 146–54.
- 72 Dunne EF,Unger ER,Sternberg M,McQuillan G,Swan DC,Patel SS,Markowitz LE. Prevalence of HPV infection among females in the United States. JAMA 2007; 297: 813–19.
- 73 Manhart LE,Holmes KK,Koutsky LA,Wood TR,Kenney DL,Feng Q,Kiviat NB. Human papillomavirus infection among sexually active young women in the United States: implications for developing a vaccination strategy. Sex Transm Dis 2006; 33: 502–8.
- 74 Partridge JM,Koutsky LA. Genital human papillomavirus infection in men. Lancet Infect Dis 2006; 6: 21–31.
- 75 WHO and EUROGIN Report on Cervical Cancer Control. European Organization Genital Infection and Neoplasia. Oncology (Huntington) 1997; 11: 1344.
- 76 Dunne EF,Nielson CM,Stone KM,Markowitz LE,Giuliano AR. Prevalence of HPV infection among men: a systematic review of the literature. J Infect Dis 2006; 194: 1044–57.
- 77 Garnett GP,Anderson RM. Balancing sexual partnerships in an age and activity stratified model of HIV transmission in heterosexual populations. IMA J Math Appl Med Biol 1994; 11: 161–92.
- 78 Stanley M,Lowy DR,Frazer I. Chapter 12: prophylactic HPV vaccines: underlying mechanisms. Vaccine 2006; 24( Suppl 3): S106–S113.
- 79 The FUTURE II Study Group. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med 2007; 356: 1915–27.
- 80 Kitchener HC,Almonte M,Wheeler P,Desai M,Gilham C,Bailey A,Sargent A,Peto J. HPV testing in routine cervical screening: cross sectional data from the ARTISTIC trial. Br J Cancer 2006; 95: 56–61.
- 81 Wang SS,Schiffman M,Shields TS,Herrero R,Hildesheim A,Bratti MC,Sherman ME,Rodriguez AC,Castle PE,Morales J,Alfaro M,Wright T, et al. Seroprevalence of human papillomavirus-16, -18, -31, and -45 in a population-based cohort of 10000 women in Costa Rica. Br J Cancer 2003; 89: 1248–54.
- 82 Medical Services Advisory Committee. Current assessments—application 1122: automated liquid based cytology; Reference 39: Human papilloma virus—triage for PAP smears. [Internet] 2008 [cited 9 March 2008]. Available from: http://www.msac.gov.au/internet/msac/publishing.nsf/Content/ref39-1.
- 83 The Cancer Council Australia. Best practice in cervical cancer immunisation: report of a roundtable discussion about the impact of the human papillomavirus vaccine in Australia. [Internet] 2008 [cited 9 March 2008]. Available from: http://www.cancer.org.au/Home.htm.
- 84 Skinner SR,Garland SM,Stanley MA,Pitts M,Quinn MA. Human papillomavirus vaccination for the prevention of cervical neoplasia: is it appropriate to vaccinate women older than 26? Med J Aust 2008; 188: 238–42.
- 85 Gall S. Substantial impact on precancerous lesions and HPV infections through 5.5 years in women vaccinated with the HPV-16/18 L1 VLP AS04 candidate vaccine. Presented at the American Association for Cancer Research (AACR) Annual Meeting, 14–16 April 2007 (abstract no. 4900).
- 86Merck submits new cross-protection data for GARDASIL® to the FDA and seeks new indications for vaginal and vulvar cancers. Medical News Today, 19 April 2007. [Internet] 2007 [cited 26 June 2007]. Available from: http://www.medicalnewstoday.com/medicalnews.php?newsid=68235.
- 87 Bryan J,Smith J,Ruiz W,Brownlow M,Brown M,Esser M. Evaluation of antibodies induced by an HPV vaccine to cross-neutralize pseudovirions of vaccine-related HPV types. J Clin Oncol 2006; 24(18S): 15008.