Anal cytological abnormalities are poor predictors of high-grade intraepithelial neoplasia amongst HIV-positive men who have sex with men
Leon P. Botes A B , Sarah Pett B C , Andrew Carr B , Debbie Marriott B , David A. Cooper B C , Gail Matthews B C , Sonia Carbone D , Nirmala Kumaradevan D , Leo McHugh A and Richard J. Hillman A B C EA Western Sydney Sexual Health Centre, Parramatta, NSW 2150, Australia.
B Centre for Applied Medical Research, St Vincent’s Hospital, Sydney, NSW 2010, Australia.
C The Kirby Institute, University of New South Wales, Sydney, NSW 2052, Australia.
D SydPath Laboratories, St Vincent’s Hospital, Sydney, NSW 2010, Australia.
E Corresponding author. Email: richard.hillman@sydney.edu.au
Sexual Health 10(1) 9-17 https://doi.org/10.1071/SH11135
Submitted: 21 September 2011 Accepted: 8 May 2012 Published: 21 December 2012
Abstract
Background: Although anal squamous cell carcinomas (ASCC) are rare in the general community, rates of ASCC among HIV-positive men who have sex with men (MSM) approach those of major cancers in the general community, such as colorectal and lung cancers. Anal cytology and high-resolution anoscopy (HRA) have been proposed as methods for the diagnosis of high-grade anal intraepithelial neoplasia (HGAIN), the precursor of ASCC. To determine the prevalence of anal disease among HIV-positive MSM, we investigated anal cytological and histological findings in men from a large HIV clinic in Sydney, Australia. Methods: This was a single-centre study conducted between October 2008 and January 2010. Participants self-collected cytology specimens, and those yielding abnormal cytology results of atypical cells of undetermined significance, atypical cells of undetermined significance – possibly high-grade (ASC-H) and high-grade squamous intraepithelial lesions (HSIL) were offered HRA. In addition, of those yielding low-grade squamous intraepithelial lesions results, a systematically selected group (25%) were offered HRA. Results: Of the 1339 HIV-positive MSM who attended the clinic during the study period, 291 (31.8%) were finally included in the study, 262 yielded technically satisfactory cytological results and 101 (36.7%) participants underwent HRA. HGAIN was identified in 55 (54.5%) of the 101 men undergoing HRA. HGAIN was diagnosed in 28 (52.7%) without cytological ASC-H or HSIL results. Conclusions: Despite the poor correlation between anal cytological and histological findings, high levels of HGAIN were identified in HIV-positive MSM attending this clinical service.
Additional keywords: anal squamous cell carcinoma, high-grade squamous intraepithelial lesion, high-resolution anoscopy.
References
[1] Australian Institute of Health and Welfare (AIHW). Cancer in Australia: an overview, 2008. Canberra: AIHW ; 2008. Available online at http://www.aihw.gov.au/publication-detail/?id=6442472459 [verified March 2011].[2] D’Souza G, Wiley D, Li X, Chmiel J, Margolick J, Cranston R, et al Incidence and epidemiology of anal cancer in the Multicenter AIDS Cohort Study. J Acquir Immune Defic Syndr 2008; 48 491–9.
| Incidence and epidemiology of anal cancer in the Multicenter AIDS Cohort Study.Crossref | GoogleScholarGoogle Scholar |
[3] Cress R, Holly E. Incidence of anal cancer in California: increased incidence among men in San Francisco, 1973–1999. Prev Med 2003; 36 555–60.
| Incidence of anal cancer in California: increased incidence among men in San Francisco, 1973–1999.Crossref | GoogleScholarGoogle Scholar |
[4] Joseph D, Miller J, Wu X, Chen V, Morris C, Goodman M, 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 | GoogleScholarGoogle Scholar |
[5] Johnson L, Madeleine M, Newcomer L, Schwartz S, Daling J. Anal cancer incidence and survival: the surveillance, epidemiology, and end results experience, 1973–2000. Cancer 2004; 101 281–8.
| Anal cancer incidence and survival: the surveillance, epidemiology, and end results experience, 1973–2000.Crossref | GoogleScholarGoogle Scholar |
[6] 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 | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M7hs1Oqtw%3D%3D&md5=fcf13ed62ec1d3318ac9798cea8f9346CAS |
[7] Berry J, Palefsky J, Welton M. Anal cancer and its precursors in HIV positive patients: perspectives and management. Surg Oncol Clin N Am 2004; 13 1211–8.
[8] Palefsky J. HPV infection in men. Dis Markers 2007; 23 261–72.
[9] Jay N, Berry J, Hogeboom C, Holly E, Darragh T, Palefsky J. Colposcopic appearance of anal squamous intraepithelial lesions. Dis Colon Rectum 1997; 40 919–28.
| Colposcopic appearance of anal squamous intraepithelial lesions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svhtleqsQ%3D%3D&md5=a7f196a8d95e3cf95bca0dd45df9185cCAS |
[10] Melbye M, Sprogel P. Aetiological parallel between anal cancer and cervical cancer. Lancet 1991; 338 657–59.
| Aetiological parallel between anal cancer and cervical cancer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3MzlvFOnsA%3D%3D&md5=559fbe47c164ab174ae038b3abace341CAS |
[11] Anderson J, Vajdic C, Grulich A. Is screening for anal cancer warranted in homosexual men? Sex Health 2004; 1 137–40.
| Is screening for anal cancer warranted in homosexual men?Crossref | GoogleScholarGoogle Scholar |
[12] Read T, Fairly C. Should we start screening for anal squamous intra-epithelial lesions in HIV-infected homosexual men? Sex Health 2011; 8 140–2.
| Should we start screening for anal squamous intra-epithelial lesions in HIV-infected homosexual men?Crossref | GoogleScholarGoogle Scholar |
[13] International Conference on Harmonisation (ICH) Expert Working Group. ICH harmonised tripartite guideline: guideline for good clinical practice; 1996. Available at: http://www.ich.org/fileadmin/Public_Web_Site/ICH_Products/Guidelines/Efficacy/E6_R1/Step4/E6_R1__Guideline.pdf [Verified 16 November 2012]
[14] National Medical Research Council (NHMRC). Screening to prevent cervical cancer; guidelines for the management of asymptomatic women with screen detected abnormalities. Canberra: NHMRC; 2005.
[15] Berry M, Jay N, Palefsky J, Welton M. State-of-the-art of high-resolution anoscopy as a tool to manage patients at risk for anal cancer. Semin Colon Rectal Surg 2004; 15 218–26.
| State-of-the-art of high-resolution anoscopy as a tool to manage patients at risk for anal cancer.Crossref | GoogleScholarGoogle Scholar |
[16] Palefsky J. Anal cancer prevention in HIV-positive men and women. Curr Opin Oncol 2009; 21 433–8.
| Anal cancer prevention in HIV-positive men and women.Crossref | GoogleScholarGoogle Scholar |
[17] Cranston R, Darragh T, Holly E, Jay N, Berry J, Da Costa M, et al Self-collected versus clinician-collected anal cytology specimens to diagnose anal intraepithelial neoplasia in HIV-positive men. J Acquir Immune Defic Syndr 2004; 36 915–20.
| Self-collected versus clinician-collected anal cytology specimens to diagnose anal intraepithelial neoplasia in HIV-positive men.Crossref | GoogleScholarGoogle Scholar |
[18] Cranston R, Hart S, Gornbein J, Hirschowitz S, Cortina G, Moe A. The prevalence, and predictive value, of abnormal anal cytology to diagnose anal dysplasia in a population of HIV-positive men who have sex with men. Int J STD AIDS 2007; 18 77–80.
| The prevalence, and predictive value, of abnormal anal cytology to diagnose anal dysplasia in a population of HIV-positive men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7jt1WlsA%3D%3D&md5=25fa3393bd97ac4a893d9d7ab891317bCAS |
[19] Williams V, Metcalf C, French M, McCloskey J. Audit of paired anal cytology and histopathology outcomes in patients referred to a public sexual health clinic. Sex Health 2010; 7 346–51.
| Audit of paired anal cytology and histopathology outcomes in patients referred to a public sexual health clinic.Crossref | GoogleScholarGoogle Scholar |
[20] Weis S, Vecino I, Pogoda J, Susa J, Nevoit J, Radaford D, et al Prevalence of anal intraepithelial neoplasia defined by anal cytology screening and high-resolution anoscopy in a primary care population of HIV-infected men and women. Dis Colon Rectum 2011; 54 433–41.
| Prevalence of anal intraepithelial neoplasia defined by anal cytology screening and high-resolution anoscopy in a primary care population of HIV-infected men and women.Crossref | GoogleScholarGoogle Scholar |
[21] Lampinen T, Miller M, Chan K, Anema A, Van Niekerk D, Schilder A, et al Randomized clinical evaluation of self-screening for anal cancer precursors in men who have sex with men. Cytojournal 2006; 3 1–7.
[22] Pineda C, Berry J, Jay N, Palefsky J, Welton M. High resolution anoscopy in the planned staged treatment of anal squamous intraepithelial lesions in HIV-negative patients. J Gastrointest Surg 2007; 11 1410–6.
| High resolution anoscopy in the planned staged treatment of anal squamous intraepithelial lesions in HIV-negative patients.Crossref | GoogleScholarGoogle Scholar |
[23] Pineda C, Berry J, Jay N, Palefsky J, Welton M. High-resolution anoscopy targeted surgical destruction of anal high-grade squamous intraepithelial lesions: a ten-year experience. Dis Colon Rectum 2008; 51 829–37.
| High-resolution anoscopy targeted surgical destruction of anal high-grade squamous intraepithelial lesions: a ten-year experience.Crossref | GoogleScholarGoogle Scholar |
[24] Palefsky J, Rubin M. The epidemiology of anal human papillomavirus and related neoplasia. Obstet Gynecol Clin North Am 2009; 36 187–200.
| The epidemiology of anal human papillomavirus and related neoplasia.Crossref | GoogleScholarGoogle Scholar |
[25] Klencke B, Palefsky J. Anal cancer: an HIV-associated cancer. Hematol Oncol Clin North Am 2003; 17 859–72.
| Anal cancer: an HIV-associated cancer.Crossref | GoogleScholarGoogle Scholar |
[26] de Pokomandy A, Rouleau D, Ghattas G, Trottier H, Vezina S, Cote P, et al HAART and progression to high-grade anal intraepithelial neoplasia in men who have sex with men and are infected with HIV. Clin Infect Dis 2011; 52 1174–81.
| HAART and progression to high-grade anal intraepithelial neoplasia in men who have sex with men and are infected with HIV.Crossref | GoogleScholarGoogle Scholar |
[27] Chin-Hong P, Palefsky J. 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 |
[28] Machalek D, Poynten I, Jin F, Fairley C, Farnsworth A, Garland S, et al Anal human papillomavirus infection, and associated neoplastic lesions in homosexual men: systematic review and meta-analysis. Lancet Oncol 2012;
| Anal human papillomavirus infection, and associated neoplastic lesions in homosexual men: systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar |
