Sexual Health Sexual Health Society
Publishing on sexual health from the widest perspective
RESEARCH ARTICLE

The epidemiology of anal cancer

Andrew E. Grulich A E , I. Mary Poynten A , Dorothy A. Machalek A , Fengyi Jin A , David J. Templeton A B and Richard J. Hillman A C D
+ Author Affiliations
- Author Affiliations

A Kirby Institute for Infection and Immunity in Society, University of New South Wales, Sydney, NSW 2052, Australia.

B Royal Prince Alfred Sexual Health, Royal Prince Alfred Hospital, Sydney, NSW 2050, Australia.

C Sexually Transmissible Infections Research Centre, University of Sydney, Jeffery House, Parramatta, NSW 2150, Australia.

D St Vincent’s Hospital, Sydney, NSW 2010, Australia.

E Corresponding author. Email: agrulich@kirby.unsw.edu.au

Sexual Health 9(6) 504-508 https://doi.org/10.1071/SH12070
Submitted: 11 May 2012  Accepted: 4 June 2012   Published: 10 September 2012

Abstract

Anal cancer comprises malignancies of the anal canal principally of two morphologic variants: squamous cell carcinoma (SCC) and adenocarcinoma. In most settings, SCC compromises more than 70% of cases. In the general population, anal cancer is uncommon, with age-standardised incidence rates mostly between 1 and 2 per 100 000 per year. However, incidence of anal SCC is increasing by 1–3% per year in developed country settings. High-risk human papillomavirus (HPV) types can be detected in 80–90% of all anal SCC cases, making it second only to cervical cancer in the closeness of its association with this virus. HPV-16 can be detected in ~90% of HPV-positive cases of anal SCC. Case–control studies have demonstrated that sexual risk factors (homosexuality in men and multiple sexual partners in women) are strongly associated with anal cancer risk. Other risk factors include immune deficiency and tobacco exposure. Anal cancer rates are highest in homosexual men, particularly in those who are HIV-positive, in whom anal cancer is among the most common of all cancers. Vaccination against HPV holds great promise for anal cancer prevention for those not already HPV-infected. For the current generation of adult high-risk populations, screening programs to allow early detection and treatment are under investigation.

Additional keywords: adenocarcinoma, homosexual, human papillomavirus, squamous cell carcinoma.


References

[1]  Jin F, Stein AN, Conway EL, Regan DG, Law M, Brotherton JM, et al Trends in anal cancer in Australia, 1982–2005. Vaccine 2011; 29 2322–7.
Trends in anal cancer in Australia, 1982–2005.CrossRef | 21255682PubMed |

[2]  Machalek DA, Poynten M, Jin F, Fairley CK, Farnsworth A, Garland SM, et al Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis. Lancet Oncol 2012; 13 487–500.
Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis.CrossRef | 22445259PubMed |

[3]  Palefsky JM, Giuliano AR, Goldstone S, Moreira ED, Aranda C, Jessen H, et al HPV vaccine against anal HPV infection and anal intraepithelial neoplasia. N Engl J Med 2011; 365 1576–85.
HPV vaccine against anal HPV infection and anal intraepithelial neoplasia.CrossRef | 1:CAS:528:DC%2BC3MXhsVSrsrbN&md5=5aa2abd713524740622154793fcda290CAS | 22029979PubMed |

[4]  Leonard D, Beddy D, Dozois EJ. Neoplasms of anal canal and perianal skin. Clin Colon Rectal Surg 2011; 24 54–63.
Neoplasms of anal canal and perianal skin.CrossRef | 22379406PubMed |

[5]  Welton MLR, Bosman F. Chapter 9. Tumours of the anal canal. In Bosman F CF, Hruban R, Theise N, editors. WHO classification of tumours of the digestive system. 4th edition. Lyon: International Agency for Research on Cancer; 2010.

[6]  Frisch M. Anal cancer. In Schottenfeld D and Fraumeni JF, editors. Cancer epidemiology and prevention. 3rd editon. New York: Oxford University Press; 2006. pp. 831–40.

[7]  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.
Understanding the burden of human papillomavirus-associated anal cancers in the US.CrossRef | 18980293PubMed |

[8]  Brewster DH, Bhatti LA. Increasing incidence of squamous cell carcinoma of the anus in Scotland, 1975–2002. Br J Cancer 2006; 95 87–90.
Increasing incidence of squamous cell carcinoma of the anus in Scotland, 1975–2002.CrossRef | 1:STN:280:DC%2BD28zos1ynsQ%3D%3D&md5=9fd6102fe045700cc5618102f0db1630CAS | 16721368PubMed |

[9]  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.
Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer.CrossRef | 15241823PubMed |

[10]  Hartwig S, Syrjanen S, Dominiak-Felden G, Brotons M, Castellsague X. Estimation of the epidemiological burden of human papillomavirus-related cancers and non-malignant diseases in men in Europe: a review. BMC Cancer 2012; 12 30
Estimation of the epidemiological burden of human papillomavirus-related cancers and non-malignant diseases in men in Europe: a review.CrossRef | 22260541PubMed |

[11]  Frisch M, Melbye M, Moller H. Trends in incidence of anal cancer in Denmark. Br Med J 1993; 306 419–22.
| 1:STN:280:DyaK3s3hsVCgtw%3D%3D&md5=c1df2d004dd4441f762ac5760fe21b4cCAS |

[12]  Nielsen A, Munk C, Kjaer SK. Trends in incidence of anal cancer and high-grade anal intraepithelial neoplasia in Denmark, 1978–2008. Int J Cancer 2012; 130 1168–73.
Trends in incidence of anal cancer and high-grade anal intraepithelial neoplasia in Denmark, 1978–2008.CrossRef | 1:CAS:528:DC%2BC3MXhs1CnsrnP&md5=80e3cf2a9f7bb671d99eaf81275d1a0fCAS | 21469144PubMed |

[13]  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.
An analysis of temporal and generational trends in the incidence of anal and other HPV-related cancers in southeast England.CrossRef | 1:STN:280:DC%2BD1M7hs1Oqtw%3D%3D&md5=fcf13ed62ec1d3318ac9798cea8f9346CAS | 19156144PubMed |

[14]  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.
Sexual practices, sexually transmitted diseases, and the incidence of anal cancer.CrossRef | 1:STN:280:DyaL1c%2FhsVSgtg%3D%3D&md5=651553935aeed99ac143a7b52879ed1bCAS | 2821396PubMed |

[15]  Holly EA, Whittemore AS, Aston DA, Ahn DK, Nickoloff BJ, Kristiansen JJ. Anal cancer incidence: genital warts, anal fissure or fistula, hemorrhoids, and smoking. J Natl Cancer Inst 1989; 81 1726–31.
Anal cancer incidence: genital warts, anal fissure or fistula, hemorrhoids, and smoking.CrossRef | 1:STN:280:DyaK3c%2FktVOluw%3D%3D&md5=b539ceb16cabc7da73c74ceb420ffe07CAS | 2810388PubMed |

[16]  Frisch M, Glimelius B, van den Brule AJ, Wohlfahrt J, Meijer CJ, Walboomers JM, et al Sexually transmitted infection as a cause of anal cancer. N Engl J Med 1997; 337 1350–8.
Sexually transmitted infection as a cause of anal cancer.CrossRef | 1:STN:280:DyaK1c%2FgtVSjtg%3D%3D&md5=85b48368c0091b3841291d9bd7f8096cCAS | 9358129PubMed |

[17]  Tseng HF, Morgenstern H, Mack TM, Peters RK. Risk factors for anal cancer: results of a population-based case–control study. Cancer Causes Control 2003; 14 837–46.
Risk factors for anal cancer: results of a population-based case–control study.CrossRef | 14682441PubMed |

[18]  Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al A review of human carcinogens – part B: biological agents. Lancet Oncol 2009; 10 321–2.
A review of human carcinogens – part B: biological agents.CrossRef | 19350698PubMed |

[19]  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.
Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta-analysis.CrossRef | 1:CAS:528:DC%2BD1MXivVars74%3D&md5=1ac1525531c054ca2c735a8bc85056aaCAS | 19115209PubMed |

[20]  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.
Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions.CrossRef | 1:CAS:528:DC%2BD1MXltFaqtrk%3D&md5=134bfbdcad1e4cb8d06432e7489283e9CAS | 19189402PubMed |

[21]  Daling JR, Weiss NS, Klopfenstein LL, Cochran LE, Chow WH, Daifuku R. Correlates of homosexual behavior and the incidence of anal cancer. JAMA 1982; 247 1988–90.
Correlates of homosexual behavior and the incidence of anal cancer.CrossRef | 1:STN:280:DyaL387ksFyrtA%3D%3D&md5=557c5c89ef4d86bdfee1ed90e458db3cCAS | 7062503PubMed |

[22]  Melbye M, Rabkin C, Frisch M, Biggar RJ. Changing patterns of anal cancer incidence in the United States, 1940–1989. Am J Epidemiol 1994; 139 772–80.
| 1:STN:280:DyaK2c3jsVWjtA%3D%3D&md5=5f97cb1437a89a55041c20a6869508efCAS | 8178790PubMed |

[23]  Scholefield JH, Thornton Jones H, Cuzick J, Northover JM. Anal cancer and marital status. Br J Cancer 1990; 62 286–8.
Anal cancer and marital status.CrossRef | 1:STN:280:DyaK3czlt1ahtQ%3D%3D&md5=fee405c38c0253d92937e70cb3a5dc6cCAS | 2386745PubMed |

[24]  Jin F, Prestage GP, Kippax SC, Pell CM, Donovan B, Templeton DJ, et al Risk factors for genital and anal warts in a prospective cohort of HIV-negative homosexual men: the HIM study. Sex Transm Dis 2007; 34 488–93.
| 17108849PubMed |

[25]  Jin F, Prestage GP, Mao L, Kippax SC, Pell CM, Donovan B, et al Incidence and risk factors for urethral and anal gonorrhoea and chlamydia in a cohort of HIV-negative homosexual men: the Health in Men Study. Sex Transm Infect 2007; 83 113–9.
Incidence and risk factors for urethral and anal gonorrhoea and chlamydia in a cohort of HIV-negative homosexual men: the Health in Men Study.CrossRef | 1:STN:280:DC%2BD2s3it12ltQ%3D%3D&md5=04519ed803b7fbc927aa8e55f2d584aaCAS | 17005541PubMed |

[26]  Sonnex C, Strauss S, Gray JJ. Detection of human papillomavirus DNA on the fingers of patients with genital warts. Sex Transm Infect 1999; 75 317–9.
Detection of human papillomavirus DNA on the fingers of patients with genital warts.CrossRef | 1:STN:280:DC%2BD3c%2FotlOhug%3D%3D&md5=02d5fb40c27c883b8f3fbfe7d496e504CAS | 10616355PubMed |

[27]  Holmes F, Borek D, Owen-Kummer M, Hassanein R, Fishback J, Behbehani A, et al Anal cancer in women. Gastroenterology 1988; 95 107–11.
| 1:STN:280:DyaL1c3isFyqtQ%3D%3D&md5=f264a63a4ceee1c71d8eeb639d2658aaCAS | 2836255PubMed |

[28]  Goodman MT, Shvetsov YB, McDuffie K, Wilkens LR, Zhu X, Ning L, et al Acquisition of anal human papillomavirus (HPV) infection in women: the Hawaii HPV Cohort study. J Infect Dis 2008; 197 957–66.
Acquisition of anal human papillomavirus (HPV) infection in women: the Hawaii HPV Cohort study.CrossRef | 18429348PubMed |

[29]  Edgren G, Sparen P. Risk of anogenital cancer after diagnosis of cervical intraepithelial neoplasia: a prospective population-based study. Lancet Oncol 2007; 8 311–6.
Risk of anogenital cancer after diagnosis of cervical intraepithelial neoplasia: a prospective population-based study.CrossRef | 17395104PubMed |

[30]  Saleem AM, Paulus JK, Shapter AP, Baxter NN, Roberts PL, Ricciardi R. Risk of anal cancer in a cohort with human papillomavirus-related gynecologic neoplasm. Obstet Gynecol 2011; 117 643–9.
Risk of anal cancer in a cohort with human papillomavirus-related gynecologic neoplasm.CrossRef | 21343768PubMed |

[31]  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.
Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis.CrossRef | 17617273PubMed |

[32]  Chaturvedi AK, Madeleine MM, Biggar RJ, Engels EA. Risk of human papillomavirus-associated cancers among persons with AIDS. J Natl Cancer Inst 2009; 101 1120–30.
Risk of human papillomavirus-associated cancers among persons with AIDS.CrossRef | 19648510PubMed |

[33]  Silverberg MJ, Lau B, Justice AC, Engels E, Gill MJ, Goedert JJ, et al Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clin Infect Dis 2012; 54 1026–34.
Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America.CrossRef | 22291097PubMed |

[34]  Silverberg MJ, Chao C, Leyden WA, Xu L, Horberg MA, Klein D, et al HIV infection, immunodeficiency, viral replication, and the risk of cancer. Cancer Epidemiol Biomarkers Prev 2011; 20 2551–9.
HIV infection, immunodeficiency, viral replication, and the risk of cancer.CrossRef | 1:CAS:528:DC%2BC3MXhsFyksr%2FI&md5=70d7081425a6835ec261d7bb59e1aed4CAS | 22109347PubMed |

[35]  Guiguet M, Boue F, Cadranel J, Lang JM, Rosenthal E, Costagliola D. Effect of immunodeficiency, HIV viral load, and antiretroviral therapy on the risk of individual malignancies (FHDH-ANRS CO4): a prospective cohort study. Lancet Oncol 2009; 10 1152–9.
Effect of immunodeficiency, HIV viral load, and antiretroviral therapy on the risk of individual malignancies (FHDH-ANRS CO4): a prospective cohort study.CrossRef | 1:CAS:528:DC%2BD1MXhsV2lurrO&md5=0b56d653c9e878e20be42142b78493b8CAS | 19818686PubMed |

[36]  Sunesen KG, Norgaard M, Thorlacius-Ussing O, Laurberg S. Immunosuppressive disorders and risk of anal squamous cell carcinoma: a nationwide cohort study in Denmark, 1978–2005. Int J Cancer 2010; 127 675–84.
Immunosuppressive disorders and risk of anal squamous cell carcinoma: a nationwide cohort study in Denmark, 1978–2005.CrossRef | 1:CAS:528:DC%2BC3cXmslSntL4%3D&md5=f5236c73270cf2c63a90451a5b97d0d9CAS | 19960431PubMed |

[37]  Phillips AN, Smith GD. Cigarette smoking as a potential cause of cervical cancer: has confounding been controlled? Int J Epidemiol 1994; 23 42–9.
Cigarette smoking as a potential cause of cervical cancer: has confounding been controlled?CrossRef | 1:STN:280:DyaK2c3lt1OktA%3D%3D&md5=2007c62f49ecebf92bdba795acf73a9dCAS | 8194922PubMed |

[38]  Appleby P, Beral V, Berrington de Gonzalez A, Colin D, Franceschi S, Goodill A, et al Carcinoma of the cervix and tobacco smoking: collaborative reanalysis of individual data on 13,541 women with carcinoma of the cervix and 23,017 women without carcinoma of the cervix from 23 epidemiological studies. Int J Cancer 2006; 118 1481–95.
Carcinoma of the cervix and tobacco smoking: collaborative reanalysis of individual data on 13,541 women with carcinoma of the cervix and 23,017 women without carcinoma of the cervix from 23 epidemiological studies.CrossRef | 1:STN:280:DC%2BD28%2FkvFCmsw%3D%3D&md5=868ddea6b04ca9131a78d79edbd5c3f7CAS | 16206285PubMed |

[39]  Frisch M, Glimelius B, Wohlfahrt J, Adami HO, Melbye M. Tobacco smoking as a risk factor in anal carcinoma: an antiestrogenic mechanism? J Natl Cancer Inst 1999; 91 708–15.
Tobacco smoking as a risk factor in anal carcinoma: an antiestrogenic mechanism?CrossRef | 1:STN:280:DyaK1M3jt1yktQ%3D%3D&md5=beb16878251d61c29636c3eeee615986CAS | 10218509PubMed |



Rent Article (via Deepdyve) Export Citation Cited By (35)

View Altmetrics