Sexually Transmitted Diseases:
Routine Anal Cytology Screening for Anal Squamous Intraepithelial Lesions in an Urban HIV Clinic
Scott, Hyman MD*; Khoury, Joe MD†; Moore, Brent A. PhD*; Weissman, Sharon MD†
From the *Yale University School of Medicine; and †Department of Medicine, Section of Infectious Disease, Hospital of Saint Raphael, New Haven, Connecticut.
Correspondence: Hyman Scott, MD, Hospital of Saint Raphael, 1450 Chapel Str., New Haven, CT. E-mail: firstname.lastname@example.org.
Address Reprint Requests: Sharon Weissman, MD, Hospital of Saint Raphael, 1450 Chapel Str., New Haven, CT.
Received for publication March 24, 2006, and accepted September 9, 2007.
Objectives: The purpose of this study is to describe our experience with routine anal cancer screening using anal cytology, determine risk factors for abnormal anal cytology, and determine if an association exists between cytology and histology in patients with HIV infection.
Methods: Demographics, CD4+ T-cell count, STD history, and cytology and histology data were extracted from medical charts of patients seen between November 1, 2002, and November 30, 2004. Analysis was done using χ2 for comparison of proportions and Student t test for continuous variables. Multivariate analysis was conducted using logistic regression controlling for age, race, sex, CD4+ T-cell nadir, and HIV exposure category.
Results: Overall, 276 of 560 of the clinic patients received a screening anal cytology during the study period. Of these patients, 11 were excluded from the analysis and 74 of 265 (27.9%) patients screened had an abnormal anal cytology. Mean age was 44 years, and 68% were men. Forty-nine percent were African American, 34% Caucasian, and 17% Hispanic. Those with an abnormal cytology were more likely to be Caucasian (P = 0.03), and be homosexual or bisexual (P = 0.02). They were also more likely to have a lower CD4+ nadir (142 cells/mm3 vs. 223 cells/mm3, P = 0.005) and CD4+ at time of anal cytology (353 cells/mm3 vs. 497 cells/mm3, P <0.001). Those with an abnormal anal cytology also had higher occurrence of anal disease on perianal visual inspection (30% vs. 9%, P <0.001) and were more likely to have a history of genital warts (23% vs. 12%, P = 0.02) or herpes (35% vs. 22%, P = 0.02). Two patients had anal intraepithelial neoplasia (AIN) I, 2 AIN II, 3 AIN III, and 2 squamous cell carcinoma in situ on histology. There was no apparent association between cytology and histology.
Conclusion: Routine anal cytology screening is a feasible tool to incorporate into HIV care for patients regardless of gender and HIV risk factors. Its impact on morbidity and mortality warrant further study.
ANAL CARCINOMA IS RELATIVELY rare in the general population, although the incidence of anal cancer is increasing among men, particularly among HIV-infected men who have sex with men (MSM).1 Recent studies have shown a rising incidence of anal cancer among HIV-infected men and women despite the widespread use of highly active antiretroviral therapy (HAART).2,3 The current estimated incidence of anal cancer is 37 per 100,000 among men with a history of receptive anal intercourse and is estimated to be approximately twice as high among the same group of men who have HIV.4–6 One cohort study has shown that as many as 49% of HIV-infected homosexual and bisexual men developed high-grade anal dysplasia over the course of a 4-year period compared to 17% of HIV-uninfected homosexual and bisexual men.7 As patients are living longer with HIV, it is likely that the incidence and complications from anal cancer will continue to increase in HIV-infected patients.
Anal carcinoma shares many similarities with cervical cancer in anatomy and histology as well as its association with human papillomavirus (HPV) infection.8–10 HIV-associated immunosuppression increases the risk of anal HPV detection.8,11,12 Several studies have demonstrated the association of HPV infection with increased risk of development of anal high-grade squamous intraepithelial lesions (HSIL) and low-grade intraepithelial lesions (LSIL).7,13–15 Similar to cervical cancer, these lesions are thought to be precursor lesions that can progress to invasive carcinoma among HIV-infected women.10,13
Routine cervical Papanicolaou smear screening has been associated with a significant decrease in the incidence of cervical cancer from 40–50 per 100,000 to approximately 10 per 100,000.16 Based on the success of the cervical cancer screening program, many experts have suggested that routine anal cytology screening should be performed on high-risk individuals to detect and remove precancerous anal lesions.17–19 It has been shown to be a cost-effective procedure for homosexual and bisexual men with benefit comparable to that of other preventative medical protocols used in HIV care.20,21
Although most available data on anal carcinoma are derived from homosexual and bisexual men, there is also an increased incidence of anal carcinoma among other groups.14,22 Cross-sectional studies identified 26% of HIV-infected women and 34% of HIV-infected men without a history of anal intercourse with anal dysplasia.14,23 As the majority of evidence for anal cancer screening programs is from HIV-infected MSM, there are no substantial data on anal dysplasia and anal cancer screening in a diverse population of HIV-infected patients seen in an urban HIV clinic. We started an anal cancer-screening program in response to concerns from many providers who noted an increased number of anal cancer cases. When we implemented the program, we felt that it would be important to re-examine the program in 1–2 years to determine its feasibility and barriers to implementation. Our goals are to describe our experience with a routine anal cytology screening program in an urban HIV-infected population to determine if anal disease on examination is predictive of abnormal anal cytology findings and if there is an association among abnormal cytology, abnormal histology, and abnormal anoscopy.
Materials and Methods
This study was conducted with the approval of the Institutional Review Board, Hospital of Saint Raphael (HSR) and the Human Investigations Committee, Yale School of Medicine. In November 2002, we implemented an anal cancer-screening program, using anal cytology, into our HIV clinical care. Six providers received in-service training on the anal cytology procedure and all HIV-infected patients seen at the HIV clinic at the HSR were offered anal cytology as part of routine clinical care. All samples were read by 1 pathologist at the HSR who was trained in interpreting anal cytology. Anal cytology results were reported as negative for dysplasia, atypical cells of undetermined significance (ASCUS), anal intraepithelial neoplasia (AIN) I, AIN II, or AIN III. The cytology reports interpreted as AIN were recoded as LSIL for AIN I and HSIL for AIN II and AIN III. Patients with abnormal anal cytology findings, classified as ASCUS or greater, were referred for surgical evaluation and anoscopy. We used the anal cancer screening protocol suggested by Drs. Chin-Hong and Palefsky.24 At the discretion of the surgeon, some patients received another screening anal cytology before anoscopy. Anoscopy was preformed using a high-resolution anoscope with biopsy of any obvious lesions seen with addition of 3% acetic acid. Biopsy results were reported as AIN I, AIN II, AIN III, or squamous cell carcinoma in situ (SCCIS).
Outpatient charts were reviewed for all patients seen between November 2002 and November 2004 who had an anal cytology examination. The following data were extracted: demographics [age, race, HIV risk factor(s)], CD4+ T-cell count at the time of anal cytology, CD4+ T-cell count nadir, HIV viral load at the time of anal cytology, current use and history of antiretroviral therapy (ART), history of provider diagnosed herpes simplex virus infection, and/or genital warts, anal disease on perianal visual inspection (anal disease was defined as wartlike lesions, ulcerations, and/or fissures), history and stage of cervical dysplasia for women, history of any other provider diagnosed genital-urinary disease, results of anal cytology, and results of high-resolution anoscopy findings. For patients with more than 1 anal cytology, the reason for additional anal cytology was recorded. Data for all patients with anal cytology were coded and entered into a computerized spreadsheet. Data collection was verified by nonprimary data collector on 10% of randomly selected charts. Less than 5% variation was found between the 2 data collectors.
For those patients with more than 1 anal cytology, the highest-grade cytologic abnormality was used in the analysis. Patients with insufficient cells on cytology slide or missing cytology results were excluded. Univariate analysis was done using χ2 for comparison of proportions and t tests for continuous variables using SPSS version 14.0 (Chicago, IL). Multivariate analysis was conducted using logistic regression controlling for age, race, sex, CD4+ T-cell nadir, and HIV risk factor. These variables were chosen to control for established risk factors. Comparisons were considered significant at P <0.05 (2-tailed).
Table 1 describes the study population of the 265 patients who received an anal cytology. The demographics of the patients receiving an anal cytology are reflective of the demographics of the entire clinic population. During the 2-year study period, 560 patients came for at least 1 routine clinical visit (Fig. 1). Two hundred seventy-six patients (49%) received at least 1 screening anal cytology during this time. Eleven patients were excluded from analysis: 10 for insufficient cells on the cytology slide and 1 for missing data. Ninety-two patients had more than 1 anal cytology done during the study period. Of these 92 patients, 72 patients had 2 anal cytologies, 19 had 3 anal cytologies, and 1 patient had 4 anal cytologies. Fifty-one patients had only normal repeat anal cytologies as part of annual screening. Four patients had a repeat anal cytology after an initial anal cytology showed insufficient sample. Thirty-four patients had a repeat anal cytology to follow-up on an original abnormal anal cytology. Three patients had a repeat anal cytology for an undocumented reason.
Normal Versus Abnormal Anal Cytology Comparison
Seventy-four of 265 (27.9%) subjects had at least 1 abnormal anal cytology (Fig. 1). Twenty-four (32%) had ASCUS, 45 (61%) had LSIL, and 5 (7%) had HSIL. The subjects with an abnormal anal cytology were significantly more likely to be caucasian, report MSM as their HIV risk factor, have a lower CD4+ T-cell nadir and lower CD4+ T-cell count at the time of anal cytology, and be on ART at the time of the anal cytology (Table 2). Patients with abnormal anal cytologies were also more likely have anal disease on perianal visual inspection and to have a history of herpes simplex virus or genital warts. There was no significant difference in history of cervical dysplasia between those with abnormal anal cytologies and those with normal anal cytologies among the 84 women. In the multivariate analysis, anal disease on perianal visual inspection and CD4+ T-cell count at the time of the anal cytology were significantly associated with abnormal anal cytology, with odds ratios of 2.8 (95% CI = 1.3–6.1) and 2.6 (95% CI = 1.2–5.6) respectively (Table 3).
Follow-Up of Abnormal Anal Cytology
Fifty of 74 patients (66%) with an abnormal anal cytology were referred for surgical evaluation (Fig. 2). Of the 24 patients without a surgical referral, 3 patients were diagnosed with another malignancy, 2 patients relocated out of city/state, and 1 patient was admitted to an extended care facility. Referral and follow-up data were lacking for the other 18 patients. Of the 50 patients with a referral, 7 patients did not report for their surgical evaluation. Sixteen of these patients did not receive anoscopy; 2 were unable to tolerate the anoscopy and, at the discretion of the surgeon, the remaining 14 had either an anal exam or a repeat anal cytology. Of the 27 patients who received anoscopy, 15 patients had no abnormalities seen on anoscopy and 3 patients had lesions but no biopsy was taken (1 patient was pregnant and 2 for an undocumented reason). Nine patients had lesions seen on anoscopy and histology proven anal dysplasia (Table 4). Two patients were identified with AIN I, 2 with AIN II, 3 with AIN III, and 2 patients with SCCIS.
Association Between Anal Cytology and Histology
There was no apparent association between cytology and histology findings (Table 4).
We have demonstrated an ability to institute an anal cancer screening program as part of routine HIV care in an ethnically diverse inner city setting. During the study period we screened approximately half (49%) of the clinic population that was seen for HIV care. This included screening a substantial number (32%) of women. Although current recommendations for anal cancer screening are specifically targeted toward MSM, high-grade anal dysplasia has been demonstrated in 36% of intravenous drug users who have no history of receptive anal intercourse.15 In our study we found that 22% of patients with intravenous drug use and 35% of patients with heterosexual sex as their only recorded HIV risk factor had abnormal anal cytology. This increased rate among heterosexual men and women is consistent with other published studies.14,25–27 The proportion of abnormal anal cytologies we found in men reporting having MSM as their HIV risk factor (39%) was lower than reported in other studies, which were concentrated in high-risk MSM communities.28 However, the risk factors in our study were collected retrospectively and were based on coding by providers in clinic charts. Thus, we may have underestimated the number of patients who have receptive anal intercourse. Nevertheless, our experience is more typical of a “real-world setting” in which providers often do not routinely collect an in-depth sexual history.29,30
We found that patients with an abnormal anal cytology were more likely to have anal disease on perianal visual inspection compared to those with a normal anal cytology. In the multivariate analysis, anal disease was associated with increased odds of having an abnormal anal cytology. However, only 30% of those with an abnormal anal cytology had anal disease on physical exam. The majority (70%) of patients with abnormal anal cytology findings did not have anal disease at the time of their anal cytology. In addition, 17 (9%) patients with a normal anal cytology had anal disease. One explanation for this finding is that only the perianal area is visible on examination, whereas the anal cytology samples were from within the anal canal, where anal dysplasia may occur.
The patients with an abnormal anal cytology were also more likely to have a lower CD4+ T-cell nadir and lower CD4+ T-cell count at the time of the anal cytology compared to those with a normal anal cytology. Interestingly, these patients were more likely to be on ART. This may reflect the treatment of patients' more advanced HIV disease. Although there is controversy regarding anal carcinoma's responsiveness to HAART, HAART does not appear to have an impact on anal HPV infection.15,31,32 HIV has a local immunosuppressive effect in the anal mucosa that is not responsive to HAART even with increases in systemic CD4+ T-cell counts and decrease in HIV viral load.8,33,34 This continued local immune suppression may be the mechanism via which HPV leads to anal carcinoma, as the decreased immune surveillance by dendritic cells allows transformed cells to grow unchecked.35
It has been shown previously that women with a history of cervical dysplasia are at increased risk for developing anal dysplasia. We were not able to demonstrate this in our study, but this may be because cervical Papanicolaou smear or colposcopy results were not always available. Many of the women received gynecological care at another institution and records were not available for review.
Of the 74 patients who were identified with cytologic evidence of anal dysplasia, only 27 received high-resolution anoscopy. Only 9 patients with visible lesions on anoscopy had a biopsy. This highlights many of the barriers to incorporating a cancer screening program into routine clinical care including substantial physician training and resources for anoscopy-related activities.36 The anal cytology was accepted by the patients and patients did not complain of side effects from this screening test. Yet, it was much more difficult to insure adherence with surgical anoscopy and biopsy follow-up. Barriers to surgical evaluation included patient-centered difficulties such as the perceived intolerability of the anoscopy procedure, fear of a cancer diagnosis, and difficulties with maintaining clinic appointments. Furthermore, as patients were initially referred for a surgical evaluation, there was confusion about the need and type of evaluation these patients required. Some patients were receiving high-resolution anoscopy and acetowhitening with biopsy of dysplasic lesions, while others received an anal examination or repeat anal cytology. With ongoing education to our surgical residents and scheduling the anal dysplasia follow-ups to 1 clinic day a week (2 clinic attendings), we were able to overcome this barrier.18,24,37 Lastly, even though the anal cytology was well accepted by patients, only half the patients seen were actually screened. This is at least partly due to the complexity and advanced HIV disease stage of our patients. If other more urgent medical problems were apparent, these would take priority and management of their anal disease would become a secondary or unaddressed issue. Despite these barriers, during the course of the screening program, 2 patients (0.7%) were identified with SCCIS. These 2 patients have been successfully treated with local therapy. They are currently being followed and remain disease free.
Our data does not show consistency between cytology and histology findings. The 3 patients with HSIL on cytology had no lesions seen on anoscopies and the 2 patients with SCCIS on biopsy had ASCUS and LSIL on cytology. This finding is consistent with other published reports.18,38 Palefsky et al. have shown that anal cytology screening in homosexual and bisexual men has a positive predictive value of 38% and negative predictive value of 84% when ASCUS was included as abnormal, as was done in with our study.18 The positive predictive value of the examination was driven by the higher disease prevalence in this patient population. In our study, only 38% of patients self-identified as having MSM as their HIV risk factor so the positive predictive value of the anal cytology screening program would likely be lower. Given that all the patients with high-grade lesions on histology were patients with ASCUS or LSIL, this study supports the recommendation of surgical evaluation of any patient with abnormalities, including ASCUS. One limitation is that approximately 32% of the patients with abnormal cytology did not receive anoscopy with biopsy. The majority of patients who did not receive an anoscopy were those with low-grade cytologic lesions.
In summary, we were able to incorporate anal cancer screening as part of routine HIV care in an urban HIV clinic setting with diverse HIV risk factors. We found cytologic abnormalities in patients without obvious risk factors, suggesting that anal cancer screening should be performed on all HIV-infected patients regardless of HIV risk factors and gender. The follow-up for abnormal anal cytology represents the most difficult aspect of the screening program. Our experience demonstrates some of the “real world” problems with setting up any screening program. It was difficult to get some patients to schedule or arrive for anoscopy even though they were aware of their abnormal anal cytology results. It then took several months to develop a uniform surgical evaluation for follow up of this new screening test. The estimated burden of disease is ∼146,372 men and ∼18,686 women and any widespread screening program would require substantial additional physician resources and training.36 Even in a group of physicians who are motivated to do such a screening program, there are difficulties and time involved in ensuring that everyone is appropriately trained. Any future recommendation for routine anal cancer screening for HIV-infected patients will have to take into consideration these implementation difficulties.
1. Melbye M, Rabkin C, Frisch M, et al. Changing patterns of anal cancer incidence in the United States, 1940–1989. Am J Epidemiol 1994; 139:772–780.
2. Chiao EY, Krown SE, Stier EA, et al. A population-based analysis of temporal trends in the incidence of squamous anal canal cancer in relation to the HIV epidemic. J Acquir Immun Defic Syndr 2005; 40:451–455.
3. Bower M, Powles T, Newsom-Davis T, et al. HIV-associated anal cancer: Has highly active antiretroviral therapy reduced the incidence or improved the outcome? J Acquir Immun Defic Syndr 2004; 37:1563–1565.
4. Daling J, Weiss N, Hislop T, et al. Sexual practices, sexually transmitted diseases, and the incidence of anal cancer. N Engl J Med 1987; 317:973–977.
5. Frisch M, Smith E, Grulich A, et al. Cancer in a population-based cohort of men and women in registered homosexual partnerships. Am J Epidemiol 2003; 157:966–972.
6. Frisch M, Biggar RJ, Goedert JJ. Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome. J Natl Cancer Inst 2000; 92:1500–1510.
7. Palefsky JM, Holly EA, Ralston ML, et al. 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.
8. Palefsky JM, Holly EA, Ralston ML, et al. 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; 177:361–367.
9. Frisch M, Glimelius B, van den Brule AJ, et al. Sexually transmitted infection as a cause of anal cancer. N Engl J Med 1997; 337:1350–1358.
10. Frazer I, Crapper R, Medley G, et al. Association between anorectal dysplasia, human papillomavirus, and human immunodeficiency virus infection in homosexual men. Lancet 1986; 657–660.
11. Kiviat N, Rompalo A, Bowden R, et al. Anal human papillomavirus infection among human immunodeficiency virus-seropositive and -seronegative men. J Infect Dis 1990; 162:358–361.
12. Kiviat NB, Critchlow CW, Holmes KK, et al. Association of anal dysplasia and human papillomavirus with immunosuppression and HIV infection among homosexual men. AIDS 1993; 7:43–49.
13. Palefsky JM, Holly EA, Hogeboom CJ, 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 Immun Defic Syndr Hum Retrovirol 1998; 17:314–319.
14. Piketty C, Darragh TM, Da Costa M, et al. High prevalence of anal human papillomavirus infection and anal cancer precursors among HIV-infected persons in the absence of anal intercourse. Ann Intern Med 2003; 138:453–459.
15. Wilkin TJ, Palmer S, Brudney KF, et al. Anal intraepithelial neoplasia in heterosexual and homosexual HIV-positive men with access to antiretroviral therapy. J Infect Dis 2004; 190:1685–1691.
16. Edwards BK, Brown ML, Wingo PA, et al. Annual report to the nation on the status of cancer, 1975–2002, featuring population-based trends in cancer treatment. J Natl Cancer Inst 2005; 97:1407–1427.
17. Qualters J, Lee N, Smith R, et al. Breast and cervical cancer surveillance, United States, 1973–1987. MMWR CDC Surveill Summ 1992; 41:431–433.
18. Palefsky JM, Holly EA, Hogeboom CJ, et al. Anal cytology as a screening tool for anal squamous intraepithelial lesions. J Acquir Immun Defic Syndr Hum Retrovirol 1997; 14:415–422.
19. Cranston RD, Darragh TM, Holly EA, et al. Self-collected versus clinician-collected anal cytology specimens to diagnose anal intraepithelial neoplasia in HIV-positive men. J Acquir Immun Defic Syndr 2004; 36:915–920.
20. Goldie SJ, Kuntz KM, Weinstein MC, et al. 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; 108:634–641.
21. Goldie SJ, Kuntz KM, Weinstein MC, et al. The clinical effectiveness and cost-effectiveness of screening for anal squamous intraepithelial lesions in homosexual and bisexual HIV-positive men. JAMA 1999; 281:1822–1829.
22. Ogunbiyi O, Scholefield JH, Raftery A, et al. Prevelence of anal human papillomavirus infection and intraepithelial neoplasia in renal allograft recipients. Br J Surg 1994; 81:365–367.
23. Holly EA, Ralston ML, Darragh TM, et al. Prevalence and risk factors for anal squamous intraepithelial lesions in women. J Natl Cancer Inst 2001; 93:843–849.
24. 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; 35:1127–1134.
25. Conley LJ, Ellerbrock TV, Bush TJ, et al. HIV-1 infection and risk of vulvovaginal and perianal condylomata acuminata and intraepithelial neoplasia: A prospective cohort study. Lancet 2002; 359:108–113.
26. Jamieson DJ, Paramsothy P, Cu-Uvin S, et al. Vulvar, vaginal, and perianal intraepithelial neoplasia in women with or at risk for human immunodeficiency virus. Obstet Gynecol 2006; 107:1023–1028.
27. Durante AJ, Williams AB, Da Costa M, et al. Incidence of anal cytological abnormalities in a cohort of human immunodeficiency virus-infected women. Cancer Epidemiol Biomarkers Prev 2003; 12:638–642.
28. Palefsky JM, Holly EA, Ralston ML, et al. Anal squamous intraepithelial lesions in HIV-positive and HIV-negative homosexual and bisexual men: Prevalence and risk factors. J Acquir Immun Defic Syndr Hum Retrovirol 1998; 17:320–326.
29. Margolis AD, Wolitski RJ, Parsons JT, et al. Are healthcare providers talking to HIV-seropositive patients about safer sex? AIDS 2001; 15:2335–2337.
30. De Rosa CJ, Marks G. Preventive counseling of HIV-positive men and self-disclosure of serostatus to sex partners: New opportunities for prevention. Health Psychol 1998; 17:224–231.
31. Stadler RF, Gregorcyk SG, Euhus DM, et al. Outcome of HIV-infected patients with invasive squamous-cell carcinoma of the anal canal in the era of highly active antiretroviral therapy. Dis Colon Rectum 2004; 47:1305–1309.
32. Gonzalez-Ruiz C, Heartfield W, Briggs B, et al. Anorectal pathology in HIV/AIDS-infected patients has not been impacted by highly active antiretroviral therapy. Dis Colon Rectum 2004; 47:1483–1486.
33. Sobhani I, Walker F, Aparicio T, et al. Effect of anal epidermoid cancer-related viruses on the dendritic (Langerhans') cells of the human anal mucosa. Clin Cancer Res 2002; 8:2862–2869.
34. Arany I, Evans T, Tyring SK. Tissue specific HPV expression and down regulation of local immune responses in condylomas from HIV seropositive individuals. Sex Transm Infect 1998; 74:349–353.
35. Sobhani I, Walker F, Roudot-Thoraval F, et al. Anal carcinoma: Incidence and effect of cumulative infections. AIDS 2004; 18:1561–1569.
36. Chiao EY, Giordano TP, Palefsky JM, et al. Screening HIV-infected individuals for anal cancer precursor lesions: A systematic review. Clin Infect Dis 2006; 43:223–233.
37. Chang GJ, Berry JM, Jay N, et al. Surgical treatment of high-grade anal squamous intraepithelial lesions: A prospective study. Dis Colon Rectum 2002; 45:453–458.
38. Panther LA, Wagner K, Proper J, et al. High resolution anoscopy findings for men who have sex with men: Inaccuracy of anal cytology as a predictor of histologic high-grade anal intraepithelial neoplasia and the impact of HIV serostatus. Clin Infect Dis 2004; 38:1490–1492.
This article has been cited 10 time(s).
Journal of Sex ResearchHeterosexual Anal Sexuality and Anal Sex Behaviors: A ReviewJournal of Sex Research
VaccineAnal HPV genotypes and related displasic lesions in Italian and foreign born high-risk malesVaccine
World Journal of SurgeryCurrent Understanding and Potential Immunotherapy for HIV-Associated Squamous Cell Carcinoma of the Anus (SCCA)World Journal of Surgery
Sexually Transmitted InfectionsAnal squamous intraepithelial lesions among HIV positive and HIV negative men who have sex with men in ThailandSexually Transmitted Infections
Surgical Clinics of North AmericaCondyloma and Other Infections Including Human Immunodeficiency VirusSurgical Clinics of North America
International Journal of Environmental Research and Public HealthSmoking Enhances Risk for New External Genital Warts in MenInternational Journal of Environmental Research and Public Health
Reproductive Health Matters
Anal cytology screening for lesions among HIV-positive patients
Reproductive Health Matters, 16():
Current Opinion in Infectious DiseasesHuman papillomavirus-associated diseases in HIV-infected men who have sex with menCurrent Opinion in Infectious Diseases
© Copyright 2008 American Sexually Transmitted Diseases Association