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High incidence of anal high‐grade squamous intra‐epithelial lesions among HIV‐positive and HIV‐negative homosexual and bisexual men

Palefsky, Joel M.1,2,5; Holly, Elizabeth A.3; Ralston, Mary L.3; Jay, Naomi2; Berry, J Michael2; Darragh, Teresa M.4

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Author Information

1Departments of Laboratory Medicine, University of California San Francisco, San Francisco, California, USA

2Departments of Stomatology, University of California San Francisco, San Francisco, California, USA

3Departments of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, USA

4Departments of Pathology, University of California San Francisco, San Francisco, California, USA.

5Requests for reprints to: Dr Joel Palefsky, Box 0100, Department of Laboratory Medicine, University of California San Francisco, San Francisco CA 94143, USA.

Sponsorship: Supported by grant NCI R01CA54053. These studies were carried out in the General Clinical Research Center, University of California San Francisco with funds provided by the Division of Research Resources 5 M01-RR-00079, U.S. Public Health Service.

Date of receipt: 5 June 1997; revised 28 November 1997; accepted 5 December 1997.

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Abstract

Objective: The incidence of anal cancer among homosexual men exceeds that of cervical cancer in women, and HIV-positive homosexual men may be at even higher risk than HIV-negative men. Cervical cancer is preceded by high-grade squamous intra-epithelial lesions (HSIL) and anal HSIL may similarly be the precursor to anal cancer. In this study, we describe the incidence of and risk factors for HSIL in HIV-positive and HIV-negative homosexual and bisexual men.

Design: Prospective cohort study of HIV-positive and HIV-negative homosexual men.

Setting: The University of California, San Francisco.

Patients: 346 HIV-positive and 262 HIV-negative men enrolled at baseline, 277 HIV-positive and 221 HIV-negative homosexual men followed after baseline.

Study design: A questionnaire was administered detailing lifestyle habits, medical history and sexual practices. Anal swabs for cytology and human papillomavirus studies were obtained, followed by biopsies of visible lesions. Human papillomavirus testing was performed using polymerase chain reaction (PCR) and ‘hybrid capture’. Blood was obtained for HIV testing and measurement of CD4 levels.

Main outcome measures: Incident HSIL.

Results: HIV-positive men were more likely to develop HSIL than HIV-negative men relative risk (RR), 3.7; 95% confidence interval (CI), 2.6–5.7. Life-table estimates of the 4-year incidence of HSIL was 49% (95% CI, 41–56) among HIV-positive men and 17% (95% CI, 12–23) among HIV-negative men. Among HIV-positive men, those with lower baseline CD4 counts (P = 0.007) and persistent infection with one or more human papillomavirus types, determined using PCR (P = 0.0001), were more likely to develop HSIL.

Conclusions: HIV infection, lower CD4 levels and human papillomavirus infection were associated with high rates of incident HSIL among homosexual men. However, high rates were found at all CD4 levels among HIV-positive men and among HIV-negative men.

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Introduction

The incidence rate for anal cancer among men with a history of receptive anal intercourse is several times higher than the current rate of cervical cancer in women in the United States, with an estimated incidence of 35 out of 100 000 prior to the HIV epidemic [1,2]. Anal cancer shares many biological characteristics with cervical cancer, including a similar histopathologic appearance and association with human papillomavirus (HPV) infection [3–5]. There is histopathologic similarity between cervical squamous intra-epithelial lesions, the precursor lesions to cervical cancer, and anal squamous intra-epithelial lesions and both are associated with HPV infection [4,5]. Several recent studies have shown that both anal squamous intra-epithelial lesions and anal HPV infection are more common in HIV-positive homosexual and bisexual (hereafter called homosexual) men than in HIV-negative homosexual men [6–11] raising the possibility that HIV-positive men may be at even higher risk of developing anal cancer than are HIV-negative homosexual men. Data are conflicting on the degree of excess incidence of anal cancer in HIV-positive homosexual men compared with HIV-negative homosexual men [12,13].

Whereas cervical squamous intra-epithelial lesions span a wide range of histopathologic abnormalities ranging from low-grade to high-grade, most cervical cancers are believed to arise from high-grade squamous intraepithelial lesions (HSIL). Detection of cervical HSIL through routine cytologic screening and treatment is believed to be responsible for much of the decline in the cervical cancer incidence in the last few decades. Although there are no data to demonstrate that anal HSIL directly progresses to invasive anal cancer, the strong similarities with cervical HSIL and the high incidence of anal cancer in populations known to have high rates of anal squamous intra-epithelial lesions suggest that anal HSIL is the precursor lesion for anal cancer. Little is known about the incidence and risk factors for anal HSIL in HIV-positive and HIV-negative homosexual men. This report describes the high incidence and risk factors for anal HSIL in a 4-year prospective study of HIV-positive and HIV-negative homosexual men.

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Methods

Study subjects

This study was conducted with the approval of the Committee on Human Research of the University of California, San Francisco. Homosexual and bisexual participants were recruited into this prospective cohort study between November 1991 and March 1994 from three sources: the San Francisco Men's Health study (SFMHS) [14], the San Francisco General Hospital cohort (SFGH) study [15], and at the University of California at San Francisco (UCSF) using newspaper advertisements. Three hundred and forty-six HIV-positive and 262 HIV-negative men were enrolled at baseline. At baseline and at each follow-up visit, an anal cytology sample was obtained [16]. Briefly, two Dacron (Hardwood Products, Guilford, Maine, USA) swabs were consecutively inserted for HPV testing, followed by anoscopy with colposcopic magnification after application of 3% acetic acid as described previously [17]. An anal biopsy was performed if one or more lesions were visualized with the colposcope. If more than one lesion was seen, biopsies were obtained from areas within the lesions that had different colposcopic appearances. Anal biopsies were fixed in 10% formalin and embedded in paraffin for routine histopathologic examination. Some visible lesions were not biopsied due to the patient's refusal or medical contra-indications such as recent acetylsalicylic acid intake, neutropenia (fewer than 1000 cells × 106/l), thrombocytopenia (platelet count less than 65 000 cells × 106/l), or concurrent intra- or perianal bacterial or herpes simplex virus infection.

HIV-positive subjects with normal cytology and no lesions seen at baseline anoscopy underwent anal examinations every 6 months as described above. HIV-negative subjects with normal cytology and no lesions seen at baseline were examined every 12 months to maximize subject retention. Both HIV-positive and HIV-negative subjects who had baseline anal squamous intra-epithelial lesions were examined every 3 months. All HIV-positive and HIV-negative subjects who had low-grade squamous intra-epithelial lesions (LSIL) detected at any visit were followed every 3 months thereafter. Subjects with histologically-confirmed HSIL were referred for treatment.

Three HIV-negative men seroconverted to HIV-positive during the 4-year follow-up period. One man was diagnosed with atypical squamous cells of undetermined significance (ASCUS) at baseline. At his 1-year visit he was HIV-positive and was diagnosed with LSIL. Nine months later he was diagnosed with HSIL. The two other men were normal at baseline. One was HIV-positive at his 2-year visit with a normal anal diagnosis at that time. He was followed for one more year and was normal except for one indeterminate diagnosis. The final man was HIV-positive at his 3-year visit and had ASCUS at that time. One year later he was diagnosed with LSIL. He developed HSIL at 4.5 years, but this was not included in the data analysis since it was beyond the 4-year period of analysis.

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Interpretation of anal cytology and histology

Anal cytology and histology were evaluated without knowledge of previous pathology results, HIV status of the subject, HPV DNA results, results of other diagnostic tests, or of any questionnaire data. Anal cytology results were classified as benign, ASCUS, LSIL or HSIL using current criteria for evaluation of cervical cytology [18]. Anal histology results were classified as benign, LSIL or HSIL. Subjects were classified as normal if they had benign cytology and no lesions visible at anoscopy or if they had benign cytology and a lesion that was determined to be histologically benign. If a lesion was visible at anoscopy but was not biopsied, and the accompanying cytology was normal, the diagnosis was considered indeterminate.

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Measurement of HIV status and CD4 levels

Enzyme-linked immunosorbent assay (ELISA) screening was used to determine HIV status at baseline in all subjects, and positive ELISA tests were confirmed with a Western blot assay. HIV-negative subjects were retested for HIV infection every 12 months. Different techniques were used over the course of this study to measure CD4 levels and appropriate adjustments made to correct for differences in these techniques using calibration curves that compared the results of the different methods using the same samples. For HIV-positive subjects CD4 levels were classified as greater than 500, 200–500, and less than 200 cells × 106/l.

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HPV testing

Because of its high sensitivity, polymerase chain reaction (PCR) was used in this study to detect low-level HPV infection. Since a positive PCR result does not discriminate between low-level and high-level infection, ‘hybrid capture’ (HC; Digene Diagnostics Inc., Silver Spring, Maryland, USA), a non-amplification-based test that measures high levels of HPV infection, was used in addition. The quantity of HPV DNA in the specimen can be determined by measuring the HC relative light unit (RLU) ratio, computed by dividing the chemiluminescent signal of the specimen by that obtained with a control sample containing 10 pg/ml of HPV 16 DNA.

Two hundred microlitres of specimen in Sample Transport Medium (Digene Diagnostics, Inc.,) were used for PCR and the remainder was used for HC. The PCR was performed using MY09/MY11 consensus HPV L1 primers as well as primers for amplification of the human ß-globin gene [19]. After 30 amplification cycles, 6 µl of amplification mixture were applied to a nylon membrane and probed with a biotin-labelled HPV L1 consensus probe mixture [19]. A separate membrane was probed with a biotin-labelled probe to the human ß-globin gene. Specimens positive with the HPV consensus probe mixture were then studied to determine the specific HPV type by preparing membranes as described above with 6 µl of specimen. The membranes were studied with probes to 29 different HPV types (6,11, 16, 18, 26, 31, 32, 33, 35, 39, 40, 45, 51, 52, 53, 54, 55, 56, 58, 59, 61, 66, 68, 69, 70, 73, AE2, Pap 155, Pap 291, as well as the following 10 types together in a probe mixture: HPV 2, 13, 34, 42, 57, 62, 64, 67, 72, and W13B). Specimens negative for ß-globin gene amplification were excluded from analysis. Negative controls for each experiment consisted of amplification of the solution containing all of the above components except for sample DNA. Positive controls included amplification of cloned HPV DNA. To ensure reproducibility of results, five randomly chosen specimens were amplified and blotted twice on different parts of each membrane. For analysis, the results of baseline HPV testing and testing at 12-month intervals were used for all subjects. A subject was considered always to have a specific type if he tested positive for that type on all visits for which PCR was available, never to have the type if all of his tests were negative, and sometimes to have it if he had both positive and negative tests for that type.

HC was conducted according to the manufacturer's recommendations. Two separate tests were performed on each anal specimen, consisting of 50 µl for the HPV types associated with a low risk of cervical cancer in Probe Group A (6/11/42/43/44), and 50 µl for detection of the HPV types associated with intermediate and high risk of cervical cancer in Probe Group B (16/18/31/33/35/45/51/52/56). The RLU ratio was determined for each specimen and classified as negative (< 1.0) or positive (> 1.0). For some analyses, positive specimens were divided into those with an RLU ratio of 1–10, 10−100 and > 100. A subject's HPV status using the RLU ratio was summarized as follows: negative, always < 1; low, sometimes > 1 and sometimes < 1, never > 100; medium, usually > 10, or sometimes > 100 and sometimes < 10; and high, always > 10 and sometimes > 100.

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Interview data

HIV-positive subjects were interviewed every 6 months during the study and asked about their current status regarding HIV-related diseases and conditions, medications, sexually transmitted diseases, anal conditions such as haemorrhoids and fissures, and behavioural topics such as smoking, drinking, substance use, and sexual practices that might be associated with anal disease. HIV-negative subjects were interviewed every year. A subject was categorized as exposed to the risk factor during the study if he responded affirmatively on any of the questionnaires administered to him after baseline up to and including the time of his first diagnosis of HSIL. Otherwise he was considered unexposed. For many behavioural variables, almost all subjects had engaged in the activity at least occasionally. For these potential risk factors, summary variables were developed to characterize exposure to the activity [19]. Different measures of duration and quantity of activity were used depending upon the activity.

Cutpoints were determined from the combined distributions of the HIV-positive and HIV-negative men. The summary risk factor exposure categories created by this process were used to divide study subjects into the following exposure groups during the 4-year follow- up: never, men who were not exposed to the risk factor during the 4-year follow-up; low exposure, men who occasionally engaged in the activity during the study; moderate exposure, men who engaged in the activity during most of the study; and high exposure, men who engaged in the activity throughout the study and usually engaged in it extensively.

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Statistical analysis

The subject's status at 4 years was recorded as the highest grade of anal lesion identified either by cytology or histology during the 4-year interval. If biopsy results were available, the highest grade of lesion from cytology and histology was used to determine the diagnosis. All data up to a subject's 4-year visit or diagnosis of HSIL were included. The 4-year visit was defined as the visit closest to 4 years after baseline among visits less than 4.25 years after baseline. Time to develop HSIL was defined as the time after baseline that a subject was first diagnosed with HSIL either by cytology or histology. The life-table method was used to estimate the survival curve with 1-year time intervals to describe the course of HSIL development [20]. The log-rank test was used to compare survival curves in different strata. Person-years analysis was used to evaluate potential risk factors for HSIL [21]. Length of follow-up was rounded to the nearest 0.25 years in this analysis. Person-years at risk and HSIL incidence allocation was based on a subject's most recent HIV and CD4 tests. To evaluate HPV infection and questionnaire topics, subjects were assigned to a constant rather than time-varying risk category based on overall exposure to the risk factor during the follow-up period. Subjects with usable HPV results at fewer than two visits (including baseline) were excluded from analyses involving HPV infection. The SAS statistical package was used for all data analysis [22].

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Results

The three sets of men recruited for this study had similar demographic characteristics. 91% were Caucasian not Hispanic, 7% were Hispanic, 2% were African-American, and 1% were other. Nine per cent reported 12 or fewer years of education, 54% reported 13–16 years, and 36% reported greater than 16 years of education. There were no differences between the HIV-positive and HIV-negative men by race, ethnicity or education. The mean age of the HIV-positive men was 42 years (range, 24–64 years) and the mean age of the HIV-negative men was 45 years (range, 26–73 years).

Of the 346 HIV-positive and 262 HIV-negative men originally enrolled in the study, 277 (80%) HIV-positive and 221 (84%) HIV-negative men were seen after their baseline visit. Of the 69 HIV-positive men not seen after baseline, 17 were diagnosed with HSIL at baseline, 17 were too ill to participate in the study after baseline, 14 moved out of the area or to an unknown location, and 21 declined to participate further in the study for other reasons. Of the 41 HIV-negative men not seen after baseline, one was diagnosed with HSIL at baseline, one was too ill to continue in the study, 10 moved and 29 declined to participate further.

Table 1 summarizes the cumulative incidence of HSIL among the remaining HIV-positive and HIV-negative subjects. One hundred and six of 277 (38%) HIV-positive subjects and 34 of 221 (15%) HIV-negative subjects developed HSIL during the study. Forty-seven of 90 (52%) HIV-positive subjects with LSIL progressed to HSIL during the follow-up period, as did seven of 17 (41%) HIV-negative subjects.

Table 1
Table 1
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Life-table analysis was used to compare the time course of HSIL development in HIV-positive and HIV-negative men. The 4-year incidence among all HIV-positive men was 49% [95% confidence interval (CI), 41–56]. In contrast, the 4-year incidence of HSIL among HIV-negative men was 17% (95% CI, 12–23). Figure 1 presents this analysis for HIV-positive men stratified by baseline CD4 count and for HIV-negative men. In HIV-positive men, lower baseline CD4 counts were associated with earlier development of HSIL (P = 0.007). HIV-positive men who had no anal lesions at baseline had a lower 4-year incidence of HSIL (38%) than did HIV-positive men who had an indeterminate diagnosis, ASCUS or LSIL at baseline (57%; P = 0.001). HIV-negative men who had no anal lesions at baseline had a lower 4-year incidence of HSIL (14%) than did HIV-negative men who had an indeterminate diagnosis, ASCUS or LSIL at baseline (33%) (P = 0.001).

Fig. 1
Fig. 1
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Table 2 describes the relationship between incident HSIL, HIV status and CD4 level using person-years of observation in analysis. HIV-positive men were more likely to develop HSIL than were HIV-negative men. Among HIV-positive men, the risk for incident HSIL increased with lower baseline CD4 levels.

Table 2
Table 2
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The role of HPV infection in incident HSIL was examined. HPV testing by PCR was available for 178 HIV-positive and 174 HIV-negative men, and testing by HC was available for 204 HIV-positive and 201 HIV-negative men. Table 3 presents relative risks and condfidence intervals for developing HSIL when HPV-positive using PCR and for the number of HPV types detected by PCR over time. Among both HIV-positive and HIV-negative men, consistent detection of HPV infection was associated with HSIL as was intermittent detection of HPV. A higher number of HPV types detected, whether persistent or intermittent, was associated with HSIL development in both HIV-positive and HIV-negative men. The role of individual HPV types could not be determined because of the small proportion of subjects with single HPV types. Similarly, using HC, the relative importance of A and B types in the development of HSIL was difficult to determine since 81% of the HIV-positive men were positive for both A types and B types. However, higher levels of HPV Group B RLU ratios over time were more strongly associated with incident HSIL among both HIV-positive and HIV-negative men than were higher Group A RLU ratios, suggesting a more important role for the former.

Table 3
Table 3
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Figure 2 shows the life-table estimates of the cumulative proportions for incident HSIL among HIV-positive men stratified by presence or absence of persistent HPV infection (i.e., detection of a specific HPV type at each 12-month visit) with one or more HPV types. The 4-year incidence of HSIL among HIV-positive men with persistent HPV infection was 63% (95% CI, 51–74), whereas the incidence of HSIL among men with no persistent infection was 23% (95% CI, 13–34; P = 0.0001).

Fig. 2
Fig. 2
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The relative importance of HIV status, baseline CD4 count, and HPV infection as risk factors for HSIL were evaluated using two different measurements of HPV; testing positive for HPV using PCR and presence of Group A and or B types using HC. For each comparison the reference group was HIV-negative subjects who were negative for the HPV measure used in the analysis. The highest relative risk was found for incident HSIL among HIV-positive men with CD4 counts less than 200 cells × 106/l who were positive for one or more types of HPV using PCR (Table 4). The highest relative risk was found for incident HSIL among HIV-positive men with CD4 counts less than 200 cells × 106/l who were positive for both Groups A and B using HC (Table 5). HIV-negative men with detection of both A and B groups were at a substantial risk of developing HSIL, similar to the risk of HIV-positive men with CD4 counts greater than 500 × 106cells/l. Some of the HIV-negative men developed HSIL without ever testing positive for HPV either by PCR or HC; three of 55 (5%) with no HPV detected using PCR developed HSIL, as did two of 63 (3%) with no HPV detected by HC (Tables 4 and 5).

Table 4
Table 4
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Table 5
Table 5
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Data from follow-up questionnaires on 204 HIV-positive men was used to evaluate the relationship between incident HSIL and possible behavioural and medical risk factors. New episodes of haemorrhoids since baseline (RR, 0.54; 95% CI, 0.34–0.80) and use of marijuana (RR, 0.64; 95% CI, 0.43–0.98) were associated with a reduced risk for HSIL. History of haemorrhoids at baseline only but not during follow-up was not associated with reduced risk of incident HSIL (RR, 0.97; 95% CI, 0.55–1.6). Other factors were examined and found to have RR close to unity. These included anal conditions (such as anal fissures, fistulas, anal infection or anal discharge, rectal itching or burning, use of laxatives, and constipation), history of sexually transmitted diseases other than warts (gonorrhea, chlamydia, syphilis and herpes), sexual practices (receptive anal intercourse, rimming, fisting), alcohol use, tobacco use, recreational drugs, recent sun exposure, radiography of the bowel, other AIDS-related symptoms, diseases and medications. A longer follow-up period is needed to assess the role of these factors in the development of HSIL in HIV-negative men who are still being followed.

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Discussion

These data demonstrate that the 4-year incidence of anal HSIL is high among both HIV-positive men and HIV-negative homosexual men. Thirty-eight per cent of the HIV-positive men and 17% of the HIV-negative men developed HSIL during the observation period of the study. Had it been possible to follow all HIV-positive men for the full 4 years, we estimate that 49% would have developed HSIL, based on our life table analysis. These results should be interpreted with caution since they were performed in highly sexually active urban populations with a mean age of over 40 years, and it is not known if they are applicable to the populations of homosexual men with different levels of sexual activity or at different ends of the age spectrum.

A key feature of this study was the routine use of anoscopy and biopsy of visible disease. While the diagnosis of HSIL was based on cytology or histology, 85% of the cases were histologically confirmed and the remainder were based on cytology. In a separate study of men participating in this cohort study, when HSIL was found on cytology and a biopsy was obtained from a visible lesion, 70% of these men also had HSIL on histology [23]. The biopsy may have missed the highest grade of disease in the lesion resulting in an understimate of its true grade. Conversely, we may have overestimated the incidence of HSIL if some of the cytologies were false positive for HSIL. However, the potential impact of cytologies that were false positive for HSIL would be minimal since most were confirmed histologically, and the proportion of cases of HSIL diagnosed by cytology alone was similar for the HIV positive and HIV-negative men.

In this study, the incidence of HSIL among HIV-negative men with no anal lesions at baseline may have been slightly underestimated relative to the HIV-positive men since HIV-negative men with no lesions were followed at longer time intervals than the HIV-positive men. In some of these men, development and regression of HSIL during this longer time interval may have been missed. However, once detected, HSIL rarely regresses among either HIV-positive or HIV-negative men (unpublished data) minimizing the likelihood that an HSIL case was missed in either group. In addition, differences in incident HSIL among those with ASCUS or LSIL detected at any time would not have been underestimated among HIV-negative men relative to HIV-positive men since all men with anal lesions were followed at the same intervals regardless of HIV status. Thus it is unlikely that HSIL would have been missed in this study.

Analyses of risk factors for progression of anal lesions were conducted separately for HIV-positive and HIV-negative men in the cohort because of possible biological differences between the two groups. In univariate analyses among HIV-positive men, the most important risk factors for incident HSIL included lower CD4 levels, persistent anal HPV infection, anal infection with multiple HPV types, and high-level HPV infection with the more oncogenic HPV types as determined using HC. Among HIV-negative men, the same risk factors for incident HSIL were important, with the exception of lower CD4 counts.

The role of HPV infection in incident HSIL is consistent with the association between HPV infection and anal cancer [4,5]. The observation of increased risk for incident HSIL associated with multiple HPV types suggests the possibility of cooperation between specific HPV types in disease pathogenesis. Alternatively, the higher number of types may reflect more advanced immunosuppression with higher levels of replication of HPV DNA facilitating detection of types whose level was previously below the limits of detection by PCR. The absence of HPV detection in a small number of cases of incident HSIL suggests that HPV types other than those detectable using current PCR methodology may play a role, or that HPV may not be involved in those cases.

Analyses of risk factors for incident HSIL in HIV-positive men revealed reduced relative risks for haemorrhoids and use of marijuana. Although the mechanisms of protection by these factors are not known, haemorrhoids are usually accompanied by a local inflammatory immune response that may modulate the course of HPV infection. The effect of haemorrhoids on incident HSIL was not mediated through reduced practice of receptive anal intercourse, since a higher frequency of receptive anal intercourse was not associated with incident HSIL in this study. Marijuana use has been shown in another study to be protective against non-Hodgkin's lymphoma among HIV-positive men, possible through immune modulation [24]. In addition, in our study, marijuana was used primarily as a recreational drug and was used more commonly among men with higher CD4 levels. Use of marijuana may have reflected a less advanced state of immunosuppression in this group rather than a direct effect on mitigating anal lesion progression.

Only one previous study has addressed incident HSIL [25]. In that study, men were followed for an average of 21 months and 15% of HIV-positive men and 5% of HIV-negative men with no baseline lesions developed HSIL [25]. In our study, 32% of HIV-positive men with no baseline lesions developed HSIL within 4 years and an even higher proportion of those with low-grade anal cytologic or histologic lesions progressed to HSIL. Fourteen per cent of HIV-negative men with no baseline lesion developed HSIL. The higher incidence of HSIL in our study among both HIV-positive and HIV-negative men may reflect the longer follow-up period. Among the HIV-positive men, it may also reflect a higher proportion of men with lower CD4 levels at baseline.

No studies have followed patients with untreated HSIL to determine the rate at which HSIL progresses to invasive cancer. However, the circumstantial evidence for HSIL as a precursor lesion to anal cancer is strong, and individuals with anal HSIL may be at risk for developing anal cancer. Several years may be required for HSIL to progress to invasive cancer, and the risk of progression of HSIL to cancer among HIV-positive men may have been mitigated in the past by mortality from other causes such as opportunistic infections. Protease inhibitors used for HIV infection are likely to prolong the survival of HIV-positive men [26]. Moreover, a preliminary analysis of 50 subjects with HSIL adminstered protease inhibitor therapy for at least 3 months has demonstrated that most (38 subjects, 76%) showed no regression of HSIL, while 11 (22%) regressed to LSIL and one (2%) regressed to ASCUS (unpublished data). Together these observations suggest that progression from HSIL to cancer may increase. The incidence of HSIL was high in HIV-negative men, although lower than in HIV-positive men. These HIV-negative men with HSIL may have more time for progression to cancer given the likelihood that they will have normal lifespans.

If HSIL is an anal cancer precursor, then screening protocols for anal HSIL may be of value in anal cancer prevention, in a similar manner to cervical cancer prevention protocols. As in the cervix, cytology is a useful tool to identify lesions in the anal canal [23]. Similarly, anoscopic evaluation of anal lesions using magnification and acetic acid may be used to identify HSIL lesions for biopsy and treatment [17]. Further data are needed to define optimal screening algorithms and treatment regimens for HSIL before routine screening should be implemented in high-risk populations.

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Bmc Cancer
Anal cytological abnormalities and epidemiological correlates among men who have sex with men at risk for HIV-1 infection
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International Journal of Cancer
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Cancer
Trends in the Occurrence of High-Grade Anal Intraepithelial Neoplasia in San Francisco: 2000-2009
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Ca-A Cancer Journal for Clinicians
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American Journal of Transplantation
Human Papillomavirus in Solid Organ Transplantation
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World Journal of Gastroenterology
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Antiviral Therapy
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Heard, I; Palefsky, JM; Kazatchkine, MD
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Oncologist
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Sexually Transmitted Infections
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International Journal of Cancer
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Scandinavian Journal of Infectious Diseases
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Surgeon-Journal of the Royal Colleges of Surgeons of Edinburgh and Ireland
Squamous Cell Carcinoma of the Anal Canal
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Surgeon-Journal of the Royal Colleges of Surgeons of Edinburgh and Ireland, 7(4): 232-237.

American Journal of Mens Health
Medical Treatment for Men Who Have Sex With Men and Are Living With HIV/AIDS
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Palefsky, JM; Holly, EA; Ralston, ML; Da Costa, M; Bonner, H; Jay, N; Berry, JM; Darragh, TM
Journal of Acquired Immune Deficiency Syndromes, 28(5): 422-428.

Frontiers in Bioscience
A review of human papillomavirus vaccines: From basic science to clinical trials
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Journal of Acquired Immune Deficiency Syndromes
Detection of genetic changes in anal intraepithelial neoplasia (AIN) of HIV-positive and HIV-negative men
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Advances in Cancer Research, Vol 82
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Konya, J; Dillner, J
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Xiv International AIDS Conference: Epidemiology
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Journal of the American Academy of Dermatology
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Kreuter, A; Brockmeyer, NH; Hochdorfer, B; Weissenborn, SJ; Stucker, M; Swoboda, M; Altmeyer, P; Pfister, H; Wieland, U
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American Surgeon
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Annals of Internal Medicine
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American Journal of Surgery
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AIDS Reader
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AIDS Reader
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Bulletin Du Cancer
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Clinical Infectious Diseases
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Journal of Infectious Diseases
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Journal of Infectious Diseases
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Journal of the American Academy of Dermatology
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European Journal of Obstetrics Gynecology and Reproductive Biology
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Journal of General Virology
Specific serum IgG, IgM and IgA antibodies to human papillomavirus types 6, 11, 16, 18 and 31 virus-like particles in human immunodeficiency virus-seropositive women
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Bmc Infectious Diseases
High prevalence of high risk human papillomavirus-capsid antibodies in human immunodeficiency virus-seropositive men: a serological study
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Journal of the National Cancer Institute
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British Journal of Dermatology
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Clinical Infectious Diseases
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
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Transplant International
Prevalence of anal HPV infection in solid-organ transplant patients prior to immunosuppression
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International Journal of Colorectal Disease
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International Journal of Colorectal Disease
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Jama-Journal of the American Medical Association
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Jama-Journal of the American Medical Association, 281(): 1822-1829.

European Journal of Cancer
Treatment of HIV-associated invasive anal cancer with combined chemoradiation
Cleator, S; Fife, K; Nelson, M; Gazzard, B; Phillips, R; Bower, M
European Journal of Cancer, 36(6): 754-758.

American Journal of Medicine
Cost-effectiveness of screening for anal squamous intraepithelial lesions and anal cancer in human immunodeficiency virus-negative homosexual and bisexual men
Goldie, SJ; Kuntz, KM; Weinstein, MC; Freedberg, KA; Palefsky, JM
American Journal of Medicine, 108(8): 634-641.

Seminars in Oncology
The epidemiology of acquired immunodeficiency syndrome malignancies
Goedert, JJ
Seminars in Oncology, 27(4): 390-401.

Annals of Internal Medicine
US centers for disease control and prevention guidelines for the treatment of sexually transmitted diseases: An opportunity to unify clinical and public health practice
Workowski, KA; Levine, WC; Wasserheit, JN
Annals of Internal Medicine, 137(4): 255-262.

Diseases of the Colon & Rectum
Preoperative immune status determines anal condyloma recurrence after surgical excision
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AIDS
Anal intraepithelial neoplasia in the highly active antiretroviral therapy era among HIV-positive men who have sex with men
Palefsky, JM; Holly, EA; Efirdc, JT; Da Costa, M; Jay, N; Berry, JM; Darragh, TM
AIDS, 19(): 1407-1414.

Journal of Clinical Oncology
Human immunodeficiency virus-associated squamous cell cancer of the anus: Epidemiology and outcomes in the highly active Antiretroviral therapy era
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Netherlands Journal of Medicine
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Netherlands Journal of Medicine, 66(3): 98-102.

Journal of Adolescent Health
Human Papillomavirus-Related Disease in Men: Not Just a Women's Issue
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Acta Gastro-Enterologica Belgica
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Journal of Acquired Immune Deficiency Syndromes
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Danish Medical Bulletin
On the etiology of anal squamous carcinoma
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Annals of Internal Medicine
High prevalence of anal human papillomavirus infection and anal cancer precursors among HIV-infected persons in the absence of anal intercourse
Piketty, C; Darragh, TM; Da Costa, M; Bruneval, P; Heard, I; Kazatchkine, MD; Palefsky, JM
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Archives of Surgery
Photodynamic therapy for carcinoma in situ of the anus
Webber, J; Fromm, D
Archives of Surgery, 139(3): 259-261.

Cancer
Anal cancer incidence and survival: The surveillance, epidemiology, and end results experience, 1973-2000
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Swiss Medical Weekly
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Sexually Transmitted Infections
Anal squamous intraepithelial lesions among HIV positive and HIV negative men who have sex with men in Thailand
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International Journal of Std & AIDS
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Sao Paulo Medical Journal
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Cancer Epidemiology Biomarkers & Prevention
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Infectious Disease Clinics of North America
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Dermatologic Clinics
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Hiv Medicine
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Gastroenterologie Clinique Et Biologique
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Annals of Surgical Oncology
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Sexually Transmitted Infections
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American Surgeon
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Disease Markers
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Journal of Cellular Physiology
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Asian Journal of Surgery
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Obstetrics and Gynecology Clinics of North America
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Nursing Clinics of North America
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American Journal of Medicine
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European Journal of Medical Research
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Hematology-Oncology Clinics of North America
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Oncology-New York
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Keywords:

HIV; human papillomavirus; anal cancer; anal intra-epithelial neoplasia; squamous intra-epithelial lesion; anal cytology; hybrid capture; polymerase chain reaction

© Lippincott-Raven Publishers.

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