Register      Login
Sexual Health Sexual Health Society
Publishing on sexual health from the widest perspective
REVIEW

The cost-effectiveness of screening for anal cancer in men who have sex with men: a systematic review

Kirsten Howard
+ Author Affiliations
- Author Affiliations

Sydney School of Public Health, Screening and Test Evaluation Program, University of Sydney, Sydney, NSW 2006, Australia. Email: kirsten.howard@sydney.edu.au

Sexual Health 9(6) 610-619 https://doi.org/10.1071/SH12017
Submitted: 7 February 2012  Accepted: 3 April 2012   Published: 10 August 2012

Abstract

Anal cancer is a relatively rare neoplasm, related to human papillomavirus (HPV), with an incidence that does not warrant general screening. However, as many cases occur in identifiable high-risk populations, targeting these groups may be cost-effective. Screening for anal cancer in men who have sex with men (MSM) may be appropriate, given their elevated risk of anal cancer. Examining existing cost-effectiveness analyses can help inform the design and conduct of future clinical and economic studies.

A review of the literature was performed using three databases to identify studies that assessed the cost-effectiveness of anal cancer screening in MSM. Five analyses were identified: four modelled the cost-effectiveness of cytological screening over a patient’s lifetime, and estimated final health outcomes as survival or quality adjusted survival. The fifth presented a decision analysis with intermediate health outcomes only and did not extrapolate to longer-term health outcomes.

Several factors influenced the incremental cost-effectiveness ratios. These factors were related to a paucity of primary data and included: availability of longer-term epidemiological and natural history data; availability of utility-based quality of life data from an appropriate respondent population; appropriate resource use information; and availability of information on screening adherence.

There is considerable uncertainty in model results: analyses from the United States suggest screening is almost always cost-effective; analyses from the United Kingdom suggest that screening is unlikely to be cost-effective. Uncertainty is primarily driven by data paucity; by summarising key uncertainties in existing models, this review can inform the design and conduct of future studies.

Additional keywords: economics, human papillomavirus, long-term health outcomes, modelling.


References

[1]  Spence AR, Franco EL, Ferenczy A. The role of human papilloma-viruses in cancer: evidence to date. Am J Cancer 2005; 4 49–64.
The role of human papilloma-viruses in cancer: evidence to date.Crossref | GoogleScholarGoogle Scholar |

[2]  Melbye M, Sprogel P. Aetiological parallel between anal cancer and cervical cancer. Lancet 1991; 338 657–9.
Aetiological parallel between anal cancer and cervical cancer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3MzlvFOnsA%3D%3D&md5=559fbe47c164ab174ae038b3abace341CAS | 1679474PubMed |

[3]  Australian Institute of Health and Welfare (AIHW). Cancer incidence to 2008. Canberra: AIHW; 2011. Available from: http://www.aihw.gov.au/cancer-data/ [verified January 2012].

[4]  Zeller JL, Lynm C, Glass RM. Anal cancer. JAMA 2008; 299 1980
Anal cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltFentrw%3D&md5=62c56b38c74984c76992aa77d39aa204CAS | 18430917PubMed |

[5]  D’Souza G, Wiley DJ, Li X, Chmiel JS, Margolick JB, Cranston RD, et al Incidence and epidemiology of anal cancer in the multicenter AIDS cohort study. Journal of Acquired Immune Deficiency Syndromes 2008; 48 491–9.
Incidence and epidemiology of anal cancer in the multicenter AIDS cohort study.Crossref | GoogleScholarGoogle Scholar | 18614927PubMed |

[6]  Bower M, Powles T, Newsom-Davis T, Thirlwell C, Stebbing J, Mandalia S, et al HIV-associated anal cancer: has highly active antiretroviral therapy reduced the incidence or improved the outcome? Journal of Acquired Immune Deficiency Syndromes 2004; 37 1563–5.
HIV-associated anal cancer: has highly active antiretroviral therapy reduced the incidence or improved the outcome?Crossref | GoogleScholarGoogle Scholar | 15577408PubMed |

[7]  MR Gold, JE Siegel, LB Russell, MC Weinstein editors. Cost-effectiveness in health and medicine. New York: Oxford University Press; 1996.

[8]  Drummond MF, Sculpher MJ, Torrance GW, O’Brien BJ, Stoddart GL. Methods for the economic evaluation of health care programmes. 3rd ed. Oxford, NY: Oxford University Press; 2005.

[9]  Owens DK. Analytic tools for public health decision making. Medical Decision Making 2002; 22 S3–S10.
Analytic tools for public health decision making.Crossref | GoogleScholarGoogle Scholar | 12369229PubMed |

[10]  National Institute for Health and Clinical Excellence (NICE). Guide to the methods of technology appraisal. June 2008. London: NICE; 2008. Available online at: http://www.nice.org.uk/media/b52/a7/taMethodsGuideUpdatedJune2008.pdf [verified January 2012].

[11]  Department of Health and Ageing (DoHA). Guidelines for preparing submissions to the Pharmaceutical Benefits Advisory Committee. December 2008. Canberra: DoHA; 2008. Available online at: http://www. health.gov.au/internet/main/publishing.nsf/content/pbacguidelines-index [verified January 2012].

[12]  Czoski-Murray C, Karnon J, Jones R, Smith K, Kinghorn G. Cost-effectiveness of screening high-risk HIV-positive men who have sex with men (MSM) and HIV-positive women for anal cancer. Health Technology Assessment 2010; 14 1–131.

[13]  Karnon J, Jones R, Czoski-Murray C, Smith KJ. Cost-utility analysis of screening high-risk groups for anal cancer. J Public Health (Bangkok) 2008; 30 293–304.
Cost-utility analysis of screening high-risk groups for anal cancer.Crossref | GoogleScholarGoogle Scholar |

[14]  Goldie SJ, Kuntz KM, Weinstein MC, Freedberg KA, Palefsky JM. Cost-effectiveness of screening for anal squamous intraepithelial lesions and anal cancer in human immunodeficiency virus-negative homosexual and bisexual men. Am J Med 2000; 108 634–41.
Cost-effectiveness of screening for anal squamous intraepithelial lesions and anal cancer in human immunodeficiency virus-negative homosexual and bisexual men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czhsFKkuw%3D%3D&md5=9f4a6ebb72cf5ff4301b50ed8298649cCAS | 10856411PubMed |

[15]  Goldie SJ, Kuntz KM, Weinstein MC, Freedberg KA, Welton ML, Palefsky JM. The clinical effectiveness and cost-effectiveness of screening for anal squamous intraepithelial lesions in homosexual and bisexual HIV-positive men. JAMA 1999; 281 1822–9.
The clinical effectiveness and cost-effectiveness of screening for anal squamous intraepithelial lesions in homosexual and bisexual HIV-positive men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3ntVWqtw%3D%3D&md5=c47329bf0031fbe3862cbb4f832abfa9CAS | 10340370PubMed |

[16]  Lam JM, Hoch JS, Tinmouth J, Sano M, Raboud J, Salit IE. Cost-effectiveness of screening for anal precancers in HIV-positive men. AIDS 2011; 25 635–42.
Cost-effectiveness of screening for anal precancers in HIV-positive men.Crossref | GoogleScholarGoogle Scholar | 21139488PubMed |

[17]  Palefsky JM, Holly EA, Ralston ML, Jay N, Berry JM, Darragh TM. High incidence of anal high-grade squamous intra-epithelial lesions among HIV-positive and HIV-negative homosexual and bisexual men. AIDS 1998; 12 495–503.
High incidence of anal high-grade squamous intra-epithelial lesions among HIV-positive and HIV-negative homosexual and bisexual men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3gt1Cmsg%3D%3D&md5=62ca91bfffa2ef7e7e161b4ee1d8ee1cCAS | 9543448PubMed |

[18]  Palefsky JM, Holly EA, Hogeboom CJ, Ralston ML, DaCosta MM, Botts R, et al Virologic, immunologic, and clinical parameters in the incidence and progression of anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual men. J Acquir Immune Defic Syndr Hum Retrovirol 1998; 17 314–9.
Virologic, immunologic, and clinical parameters in the incidence and progression of anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7osVensQ%3D%3D&md5=5d185f49475940ef94049f0687ea7ffdCAS | 9525431PubMed |

[19]  Palefsky JM, Holly EA, Ralston ML, Jay N. Prevalence and risk factors for human papillomavirus infection of the anal canal in human immunodeficiency virus (HIV)-positive and HIV-negative homosexual men. J Infect Dis 1998; 177 361–7.
Prevalence and risk factors for human papillomavirus infection of the anal canal in human immunodeficiency virus (HIV)-positive and HIV-negative homosexual men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7isF2qug%3D%3D&md5=9307401f9018341d4be05af9f95c5583CAS | 9466522PubMed |

[20]  Critchlow CW, Surawicz CM, Holmes KK, Kuypers J, Daling JR, Hawes SE, et al Prospective study of high grade anal squamous intraepithelial neoplasia in a cohort of homosexual men: influence of HIV infection, immunosuppression and human papillomavirus infection. AIDS 1995; 9 1255–62.
Prospective study of high grade anal squamous intraepithelial neoplasia in a cohort of homosexual men: influence of HIV infection, immunosuppression and human papillomavirus infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK287is1Wrsg%3D%3D&md5=7a7f8d247bf8843a5e842c36d03a9988CAS | 8561979PubMed |

[21]  Kiviat NB, Critchlow CW, Holmes KK, Kuypers J, Sayer J, Dunphy C, et al Association of anal dysplasia and human papillomavirus with immunosuppression and HIV infection among homosexual men. AIDS 1993; 7 43–50.
Association of anal dysplasia and human papillomavirus with immunosuppression and HIV infection among homosexual men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s7otlCgsQ%3D%3D&md5=cc39aed15be2d0d400de9495afe553d7CAS | 8382927PubMed |

[22]  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 | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c%2FhsVSgtg%3D%3D&md5=651553935aeed99ac143a7b52879ed1bCAS | 2821396PubMed |

[23]  Palefsky JM, Holly EA, Hogeboom CJ, Berry JM, Jay N, Darragh TM. Anal cytology as a screening tool for anal squamous intraepithelial lesions. J Acquir Immune Defic Syndr Hum Retrovirol 1997; 14 415–22.
Anal cytology as a screening tool for anal squamous intraepithelial lesions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szhsVSksQ%3D%3D&md5=843dc3a3960718701c4eb9321b89291cCAS | 9170415PubMed |

[24]  Peddada AV, Smith DE, Rao AR, Frost DB, Kagan AR. Chemotherapy and low-dose radiotherapy in the treatment of HIV-infected patients with carcinoma of the anal canal. Int J Radiat Oncol Biol Phys 1997; 37 1101–5.
Chemotherapy and low-dose radiotherapy in the treatment of HIV-infected patients with carcinoma of the anal canal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjvFehsrY%3D&md5=6a966510bb50980817bfd50fd9f89addCAS | 9169819PubMed |

[25]  Bottomley DM, Aqel N, Selvaratnam G, Phillips RH. Epidermoid anal cancer in HIV infected patients. Clin Oncol (R Coll Radiol) 1996; 8 319–22.
Epidermoid anal cancer in HIV infected patients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2FovVWitg%3D%3D&md5=9a8f6a4b925c43e37a541c54df92a303CAS |

[26]  Mendenhall WM, Sombeck MD, Speer TW, Marsh RD, Carroll RR, Copeland EM. Current management of squamous cell carcinoma of the anal canal. Surg Oncol 1994; 3 135–46.
Current management of squamous cell carcinoma of the anal canal.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2FktVWhsQ%3D%3D&md5=741dfec5a5248f45ab56e5d11a7d8328CAS | 7952397PubMed |

[27]  Holland JM, Swift PS. Tolerance of patients with human immunodeficiency virus and anal carcinoma to treatment with combined chemotherapy and radiation therapy. Radiology 1994; 193 251–4.
| 1:STN:280:DyaK2cznslKgug%3D%3D&md5=7e7a64b4dddb193130215e4c7754eee1CAS | 8090901PubMed |

[28]  Chadha M, Rosenblatt EA, Malamud S, Pisch J, Berson A. Squamous-cell carcinoma of the anus in HIV-positive patients. Dis Colon Rectum 1994; 37 861–5.
Squamous-cell carcinoma of the anus in HIV-positive patients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2czlslSgtg%3D%3D&md5=58ba5f290f65abcc82b9a157361f67c8CAS | 8076484PubMed |

[29]  Freedberg KA, Scharfstein JA, Seage GR, Losina E, Weinstein MC, Craven DE, et al The cost-effectiveness of preventing AIDS-related opportunistic infections. JAMA 1998; 279 130–6. [Erratum appears in JAMA 1999 Jun 2;281(21):1989]
The cost-effectiveness of preventing AIDS-related opportunistic infections.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7gtFKisQ%3D%3D&md5=dff5a6e2642a529cddc099ac4029297dCAS | 9440663PubMed |

[30]  Fryback DG, Dasbach EJ, Klein R, Klein BE, Dorn N, Peterson K, et al The Beaver Dam Health Outcomes Study: initial catalog of health-state quality factors. Med Decis Making 1993; 13 89–102.
The Beaver Dam Health Outcomes Study: initial catalog of health-state quality factors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s3kslCktw%3D%3D&md5=72ecb73287e5f09f0b4d79e186a8eb2eCAS | 8483408PubMed |

[31]  Gold MR, Franks P, McCoy KI, Fryback DG. Toward consistency in cost-utility analyses: using national measures to create condition-specific values. Med Care 1998; 36 778–92.
Toward consistency in cost-utility analyses: using national measures to create condition-specific values.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3pt1SksA%3D%3D&md5=3540170c7e5896c3825ca388e7e6b3cbCAS | 9630120PubMed |

[32]  Sayers SJ, McMillan A, McGoogan E. Anal cytological abnormalities in HIV-infected homosexual men. Int J STD AIDS 1998; 9 37–40.
Anal cytological abnormalities in HIV-infected homosexual men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7ktVGksQ%3D%3D&md5=870ec1756f7ffdab2ddd4f532ace8cd3CAS | 9518013PubMed |

[33]  Wong S, Gibbs P, Chao M, Jones I, McLaughlin S, Tjandra J, et al Carcinoma of the anal canal: a local experience and review of the literature. ANZ J Surg 2004; 74 541–6.
Carcinoma of the anal canal: a local experience and review of the literature.Crossref | GoogleScholarGoogle Scholar | 15230786PubMed |

[34]  Chang GJ, Berry JM, Jay N, Palefsky JM, Welton ML. Surgical treatment of high-grade anal squamous intraepithelial lesions: a prospective study. Dis Colon Rectum 2002; 45 453–8.
Surgical treatment of high-grade anal squamous intraepithelial lesions: a prospective study.Crossref | GoogleScholarGoogle Scholar | 12006924PubMed |

[35]  Brown SR, Skinner P, Tidy J, Smith JH, Sharp F, Hosie KB. Outcome after surgical resection for high-grade anal intraepithelial neoplasia (Bowen’s disease). Br J Surg 1999; 86 1063–6.
Outcome after surgical resection for high-grade anal intraepithelial neoplasia (Bowen’s disease).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzptVagtw%3D%3D&md5=ba1b12d6c90e08d89edb7b4bfc166af6CAS | 10460644PubMed |

[36]  Marchesa P, Fazio VW, Oliart S, Goldblum JR, Lavery IC. Perianal Bowen’s disease: a clinicopathologic study of 47 patients. Dis Colon Rectum 1997; 40 1286–93.
Perianal Bowen’s disease: a clinicopathologic study of 47 patients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FjsVSgtg%3D%3D&md5=db4f8dc6af056720c9ffb9af74999195CAS | 9369101PubMed |

[37]  Arnott SJ, Cunningham D, Gallagher J. Epidermoid anal cancer: results from the UKCCCR randomised trial of radiotherapy alone versus radiotherapy, 5-fluorouracil, and mitomycin. UKCCCR Anal Cancer Trial Working Party. UK Co-ordinating Committee on Cancer Research. Lancet 1996; 348 1049–54.

[38]  Chiao EY, Giordano TP, Palefsky JM, Tyring S, El SH. Screening HIV-infected individuals for anal cancer precursor lesions: a systematic review. Clin Infect Dis 2006; 43 223–33.
Screening HIV-infected individuals for anal cancer precursor lesions: a systematic review.Crossref | GoogleScholarGoogle Scholar | 16779751PubMed |

[39]  Cranston RD, Darragh TM, Holly EA, Jay N, Berry JM, Da CM, et al Self-collected versus clinician-collected anal cytology specimens to diagnose anal intraepithelial neoplasia in HIV-positive men. Journal of Acquired Immune Deficiency Syndromes 2004; 36 915–20.
Self-collected versus clinician-collected anal cytology specimens to diagnose anal intraepithelial neoplasia in HIV-positive men.Crossref | GoogleScholarGoogle Scholar | 15220697PubMed |

[40]  Arain S, Walts AE, Thomas P, Bose S. The anal Pap smear: cytomorphology of squamous intraepithelial lesions. Cytojournal 2005; 2 4
The anal Pap smear: cytomorphology of squamous intraepithelial lesions.Crossref | GoogleScholarGoogle Scholar | 15715910PubMed |

[41]  Goldie SJ, Freedberg KA, Weinstein MC, Wright TC, Kuntz KM. Cost effectiveness of human papillomavirus testing to augment cervical cancer screening in women infected with the human immunodeficiency virus. Am J Med 2001; 111 140–9.
Cost effectiveness of human papillomavirus testing to augment cervical cancer screening in women infected with the human immunodeficiency virus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mvlt1Shsg%3D%3D&md5=6f1982b713b7e80fcf9700643d0cfafaCAS | 11498068PubMed |

[42]  Trueman P, Youle M, Sabin CA, Miners AH, Beck EJ. The cost-effectiveness of triple nucleoside analogue therapy antiretroviral regimens in the treatment of HIV in the United Kingdom. HIV Clin Trials 2000; 1 27–35.
The cost-effectiveness of triple nucleoside analogue therapy antiretroviral regimens in the treatment of HIV in the United Kingdom.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrktlKrtQ%3D%3D&md5=8cce1367c949ad97119578d15ca626c6CAS | 11590487PubMed |

[43]  Mauskopf J, Lacey L, Kempel A, Simpson K. The cost-effectiveness of treatment with lamivudine and zidovudine compared with zidovudine alone: a comparison of Markov model and trial data estimates. Am J Manag Care 1998; 4 1004–12.
| 1:STN:280:DyaK1czotFKjuw%3D%3D&md5=1d2ab03ae6ebb7a0b46fd087f82cdec8CAS | 10181990PubMed |

[44]  Palefsky JM, Holly EA, Ralston ML, Arthur SP, Jay N, Berry JM, et al Anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual and bisexual men: prevalence and risk factors. J Acquir Immune Defic Syndr Hum Retrovirol 1998; 17 320–6.
Anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual and bisexual men: prevalence and risk factors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7osVentg%3D%3D&md5=836987e9a63dc0fd9802b69397daa436CAS | 9525432PubMed |

[45]  Chin-Hong PV, Palefsky JM. Natural history and clinical management of anal human papillomavirus disease in men and women infected with human immunodeficiency virus. Clin Infect Dis 2002; 35 1127–34.
Natural history and clinical management of anal human papillomavirus disease in men and women infected with human immunodeficiency virus.Crossref | GoogleScholarGoogle Scholar | 12384848PubMed |

[46]  Howard K, Salkeld G, Irwig L, Adelstein BA. High participation rates are not necessary for cost-effective colorectal cancer screening. J Med Screen 2005; 12 96–102.
High participation rates are not necessary for cost-effective colorectal cancer screening.Crossref | GoogleScholarGoogle Scholar | 15949121PubMed |

[47]  Salit IE, Lytwyn A, Raboud J, Sano M, Chong S, Diong C, et al The role of cytology (Pap tests) and human papillomavirus testing in anal cancer screening. AIDS 2010; 24 1307–13.
| 20442633PubMed |

[48]  Lytwyn A, Salit IE, Raboud J, Chapman W, Darragh T, Winkler B, et al Interobserver agreement in the interpretation of anal intraepithelial neoplasia. Cancer 2005; 103 1447–56.
Interobserver agreement in the interpretation of anal intraepithelial neoplasia.Crossref | GoogleScholarGoogle Scholar | 15726546PubMed |