Cancers attributable to human papillomavirus infection
Andrew E. Grulich A E , Fengyi Jin A B , E. Lynne Conway C , Alicia N. Stein C and Jane Hocking DA HIV Epidemiology and Prevention Program, National Centre in HIV Epidemiology and Clinical Research, University of New South Wales, Sydney, NSW 2021, Australia.
B Sexually Transmitted Infections Research Centre, University of Sydney, NSW 2006, Australia.
C CSL Limited, Parkville, Vic. 3052, Australia.
D School of Population Health, University of Melbourne, Carlton, Vic. 2010, Australia.
E Corresponding author. Email: agrulich@nchecr.unsw.edu.au
Sexual Health 7(3) 244-252 https://doi.org/10.1071/SH10020
Submitted: 18 February 2010 Accepted: 19 April 2010 Published: 19 August 2010
Abstract
Although the human papillomavirus (HPV) vaccine was introduced primarily as a cervical cancer prevention vaccine, HPV has a causal role in several types of cancer. This article reviews the epidemiological evidence for the role of HPV in human cancer, and describes Australian trends in these cancers. HPV is a necessary cause of cervical cancer. The currently vaccine-preventable subtypes of HPV 16 and 18 are responsible for ~70% of cervical cancer. The introduction of an organised Pap smear program in Australia led to a steep decline in incidence over the past decades. HPV can be detected in ~40% and 70% of vulval and vaginal cancers respectively. Rates of these cancers have been stable over the past 20 years. The prevalence of HPV in penile cancer is ~50% and incidence has not recently changed. For anal cancer, ~85% of cases are HPV positive, and incidence has increased significantly in both men and women over the past 20 years. In the oral cavity, ~35% of oropharyngeal cancers and ~25% of other oral cavity cancers are HPV positive. The incidence of HPV-related oral cavity and oropharyngeal cancers is increasing, whereas incidence at HPV-unrelated sites is decreasing. Overall, 1154 HPV-related cancer cases were potentially preventable by vaccination. If HPV-related cancers at non-cervical sites are prevented by vaccination, then a similar number of cancer cases will be prevented as in the cervix. However, almost one-quarter of the potentially preventable cancer cases are in men, who are not included in the current national immunisation program.
Additional keywords: Australia, cervical cancer, HPV vaccine.
[1] Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, Ghissassi F, et al. A review of human carcinogens – part B: biological agents. Lancet Oncol 2009; 10 321–2.
| Crossref | GoogleScholarGoogle Scholar | PubMed | [verified May 2010].
[7]
[8] Wain GV. Cervical cancer prevention: the saga goes on, but so much has changed! Med J Aust 2006; 185 476–7.
| PubMed | [verified May 2010].
[11] Chan PK, Chang AR, Yu MY, Li W-H, Chan MYM, Yeung ACM, et al. Age distribution of human papillomavirus infection and cervical neoplasia reflects caveats of cervical screening policies. Int J Cancer 2010; 126 297–301.
| Crossref | GoogleScholarGoogle Scholar | PubMed | [verified May 2010].
[31] De Vuyst H, Clifford GM, Nascimento MC, Madeleine MM, Franceschi S. Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta-analysis. Int J Cancer 2009; 124 1626–36.
| Crossref | GoogleScholarGoogle Scholar | PubMed | [verified May 2010].
[34] Condon JR, Rumbold AR, Thorn JC, O’Brien MM, Davy MJ, Zardawi I. A cluster of vulvar cancer and vulvar intraepithelial neoplasia in young Australian Indigenous women. Cancer Causes Control 2009; 20 67–74.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[35] Munoz N, Kjaer SK, Sigurdsson K, Iversen O-E, Hernandez-Avila M, Wheeler CM, 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; 102 325–39.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[36] Backes DM, Kurman RJ, Pimenta JM, Smith JS. Systematic review of human papillomavirus prevalence in invasive penile cancer. Cancer Causes Control 2009; 20 449–57.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[37] Bleeker MC, Heideman DA, Snijders PJ, Horenblas S, Dillner J, Meijer CJLM. Penile cancer: epidemiology, pathogenesis and prevention. World J Urol 2009; 27 141–50.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[38] Miralles-Guri C, Bruni L, Cubilla AL, Castellsagué X, Bosch FX, de Sanjosé S. Human papillomavirus prevalence and type distribution in penile carcinoma. J Clin Pathol 2009; 62 870–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[39] Auvert B, Sobngwi-Tambekou J, Cutler E, Nieuwoudt M, Lissouba P, Puren A, et al. Effect of male circumcision on the prevalence of high-risk human papillomavirus in young men: results of a randomized controlled trial conducted in Orange Farm, South Africa. J Infect Dis 2009; 199 14–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[40]
[41] Joseph DA, Miller JW, Wu X, Chen VW, Morris CR, Goodman MT, et al. Understanding the burden of human papillomavirus-associated anal cancers in the US. Cancer 2008; 113 2892–900.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[42] Franceschi S, De Vuyst H. Human papillomavirus vaccines and anal carcinoma. Curr Opin HIV and AIDS 2009; 4 57–63.
| Crossref | GoogleScholarGoogle Scholar |
[43] Robinson D, Coupland V, Moller H. An analysis of temporal and generational trends in the incidence of anal and other HPV-related cancers in Southeast England. Br J Cancer 2009; 100 527–31.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[44] Hoots BE, Palefsky JM, Pimenta JM, Smith JS. Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions. Int J Cancer 2009; 124 2375–83.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[45] Daling JR, Madeleine MM, Johnson LG, Schwartz SM, Shera KA, Wurscher MA, et al. Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer. Cancer 2004; 101 270–80.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[46] Vajdic CM, van Leeuwen MT, Jin F, Prestage G, Medley G, Hillman RJ, et al. Anal human papillomavirus genotype diversity and co-infection in a community-based sample of homosexual men. Sex Transm Infect 2009; 85 330–5.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[47] Daling JR, Weiss NS, Hislop TG, Maden C, Coates RJ, Sherman KJ, et al. Sexual practices, sexually transmitted diseases, and the incidence of anal cancer. N Engl J Med 1987; 317 973–7.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[48] Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet 2007; 370 59–67.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[49] Palefsky J. Human papillomavirus-related disease in people with HIV. Curr Opin HIV and AIDS 2009; 4 52–6.
| Crossref | GoogleScholarGoogle Scholar |
[50] van Leeuwen MT, Vajdic CM, Middleton MG, McDonald AM, Law M, Kaldor JM, et al. Continuing declines in some but not all HIV-associated cancers in Australia after widespread use of antiretroviral therapy. AIDS 2009; 23 2183–90.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[51]
[52] Anderson JS, Vajdic C, Grulich AE. Is screening for anal cancer warranted in homosexual men? Sex Health 2004; 1 137–40.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[53] Parkin DM, Louie KS, Clifford G. Burden and trends of type-specific human papillomavirus infections and related diseases in the Asia Pacific region. Vaccine 2008; 26(Suppl. 12): M1–16.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[54] Ryerson AB, Peters ES, Coughlin SS, Chen VW, Gillison ML, Reichman ME, et al. Burden of potentially human papillomavirus-associated cancers of the oropharynx and oral cavity in the US, 1998–2003. Cancer 2008; 113 2901–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[55] Sturgis EM, Cinciripini PM. Trends in head and neck cancer incidence in relation to smoking prevalence: an emerging epidemic of human papillomavirus-associated cancers? Cancer 2007; 110 1429–35.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[56] Frisch M, Hjalgrim H, Jaeger AB, Biggar RJ. Changing patterns of tonsillar squamous cell carcinoma in the United States. Cancer Causes Control 2000; 11 489–95.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[57] Näsman A, Attner P, Hammarstedt L, Du J, Eriksson M, Giraud G, et al. Incidence of human papillomavirus (HPV) positive tonsillar carcinoma in Stockholm, Sweden: an epidemic of viral-induced carcinoma? Int J Cancer 2009; 125 362–6.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[58] Kreimer AR, Clifford GM, Boyle P, Falaschini S. Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review. Cancer Epidemiol Biomarkers Prev 2005; 14 467–75.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[59] Termine N, Panzarella V, Falaschini S, Russo A, Matranga D, Lo Muzio L, et al. HPV in oral squamous cell carcinoma vs head and neck squamous cell carcinoma biopsies: a meta-analysis (1988–2007). Ann Oncol 2008; 19 1681–90.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[60] Ragin CC, Taioli E. Survival of squamous cell carcinoma of the head and neck in relation to human papillomavirus infection: review and meta-analysis. Int J Cancer 2007; 121 1813–20.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[61] D’Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, et al. Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 2007; 356 1944–56.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[62] D’Souza G, Agrawal Y, Halpern J, Bodison S, Gillison ML. Oral sexual behaviors associated with prevalent oral human papillomavirus infection. J Infect Dis 2009; 199 1263–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[63] Gillison ML, D’Souza G, Westra W, Sugar E, Xiao W, Begum S, et al. Distinct risk factor profiles for human papillomavirus type 16-positive and human papillomavirus type 16-negative head and neck cancers. J Natl Cancer Inst 2008; 100 407–20.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[64] Adelstein DJ, Ridge JA, Gillison ML, Chaturvedi AK, D’Souza G, Gravitt PE, et al. Head and neck squamous cell cancer and the human papillomavirus: summary of a National Cancer Institute State of the Science Meeting, November 9–10, 2008, Washington, D.C. Head Neck 2009; 31 1393–422.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[65] Gillison ML, Chaturvedi AK, Lowy DR. HPV prophylactic vaccines and the potential prevention of noncervical cancers in both men and women. Cancer 2008; 113 3036–46.
| Crossref | GoogleScholarGoogle Scholar | PubMed |