ABSTRACT
Background
The incidence of anal cancer has increased in the past decade, especially among men who have sex with men (MSM) and HIV-infected individuals. There is controversy about whether to routinely screen for anal cancer in MSM.
Objectives
To determine whether current anal cancer screening behaviors, intention, and concern differ by HIV serostatus and to identify characteristics of men who intend to seek anal cancer screening.
Design and Participants
Cross-sectional analysis of data collected from 901 HIV-infected and 1,016 HIV-uninfected MSM from the Multicenter AIDS Cohort Study (MACS) in 2005–2006.
Measurements
Self-reported anal cancer screening history, attitudes, and intentions.
Results
A history of anal warts was relatively common in these men (39%), whereas having a recent anal Pap test (5%), intention to seek anal cancer screening in the next 6 months (12%), and concern about anal cancer (8.5%) were less common. Intention to seek anal cancer screening was associated with enabling factors (screening availability, health insurance), need factors (HIV-infection, history of anal warts), concern about anal cancer, and recent sexual risk taking. Among four large US cities, there was significant regional variability in anal cancer screening behaviors, intention, and concern (all p<0.001). Most MSM (76%) indicated they would go to their primary care physician for an anal health problem or question.
Conclusions
This study demonstrates a low rate of anal cancer screening and intention to screen among MSM. As more evidence emerges regarding screening, primary care physicians should be prepared to discuss anal cancer screening with their patients.
KEY WORDS: anal cancer, screening, health seeking behavior, MSM, HIV infection, intention
INTRODUCTION
The incidence of anal cancer has increased in the past decade1, particularly in certain population subgroups. Both HIV-infected men and men who have sex with men (MSM) are at increased risk of anal cancer compared to the general population2–4. In fact, the rates of anal cancer among HIV-infected men are similar to the rates of cervical cancer prior to the initiation of the Pap smear screening program5. As HIV-infected men are living longer, anal cancer poses a larger long-term health issue for this population.
Human papillomavirus (HPV) infection is strongly associated with anal cancer, and those who engage in unprotected receptive anal sex are at increased risk of anal HPV infection and anal cancer6,7. Because the development of anal cancer passes through similar stages as cervical cancer, some experts recommend a similar screening strategy using anal Papanicolaou (Pap) smears to identify pre-cancerous cells and to treat them prior to the development of invasive cancer8,9. Initial model-based studies suggest that regular screening for anal cancer would increase the quality-adjusted life expectancy of HIV-infected9 and HIV-uninfected8 MSM and would be cost-effective. However, no major prevention guideline currently provides clear guidance regarding anal cancer screening, and little is known about the current proportion of men who have sought or intend to seek anal cancer screening, or from which type of health providers men will seek these services.
Identification of factors related to anal cancer screening will help inform future targeted screening efforts for high-risk men. We could identify only one study of anal cancer screening awareness in men: a report that Australian MSM had little awareness of anal cancer, anal cancer screening, or HPV10. That study was conducted at a single site in 2005 and included a small proportion (6.4%) of HIV-infected men. For this study, we surveyed men enrolled in the Multicenter AIDS Cohort Study (MACS), a large longitudinal study of HIV-infected and HIV-uninfected MSM in the US.
The study objectives were to (1) determine the prevalence of current health-care experiences related to anal cancer screening, (2) determine whether these vary by HIV serostatus, and (3) to identify factors associated with intention to seek anal cancer screening in the next 6 months among these men.
METHODS
Study Population
Participants include all men enrolled in the MACS as of visit 43 (March 2005), including 901 HIV-infected and 1,016 HIV-uninfected men. The MACS has been described in detail elsewhere11,12. In brief, the study has sites in Baltimore/Washington D.C., Los Angeles, Chicago, and Pittsburgh. Beginning in 1984, a total of 6,972 men were enrolled in three separate enrollment waves, of whom 30% were still in active follow-up at the time of analysis. Participants no longer in the study at visit 43 included those who had died (30%), been lost to follow-up (15%), or been administratively censored when the number of HIV-negative participants followed was intentionally reduced in 1993 (26%). While the vast majority of men in the study have sex with men, ~7% of the men in the study are heterosexual. IRB approval was obtained for this study at each site, and all men provided written informed consent.
Data Collection
Detailed data were collected from participants every 6 months in interviewer-administered and audio computer-assisted self interview (ACASI) format. For these analyses, we used data collected at visits 43–45 (March 2005-October 2006).
Measures Related to Anal Cancer Screening
Beginning in March 2005 (visit 43), specific questions about anal cancer screening were added to the MACS surveys. Anal wart history was measured by the question: “Have you had anal warts (condylomata acuminata) since your last visit?” and “have you ever had anal warts?” Presence or absence of anal warts was also specifically noted at each biannual physical exam. Individuals were considered to have a history of anal warts if they self reported a history and/or anal warts were observed during the physical exam. Anal Pap history was measured by the questions: “Since your last visit, have you undergone an anal Pap smear? (An anal Pap smear is collecting a sample of cells with a small brush or cotton swab to check for signs of an abnormality).” History of ever having an anal Pap smear was also collected at visit 43.
Concern about anal cancer was assessed by the question: “How concerned are you about developing anal cancer at some point in your lifetime?” Response options for this question included a five-point Likert-like scale, with responses ranging from very likely to very unlikely. Intention to seek screening for anal cancer was measured by the question: “How likely is it that you will be screened for anal cancer, anal warts, or another anal health problem in the next 6 months?", with similar response options. Perceived screening availability was assessed by the question: “Is anal cancer screening (testing involving an anal Pap smear, collection of a swab, or possible anal biopsy) available in your community?” Responses to these questions were evaluated at visit 43–45. As no trends were apparent in screening intention or concern across visits, responses at these three semi-annual visits were averaged for this analysis. Averaged intention to seek anal cancer screening was coded into categories defined as “unlikely” (1.0–2.5), “possible” (2.6–3.5), and “likely” (3.5–5.0). Similarly, averaged concern about anal cancer was coded into categories defined as “not concerned” (1.0–2.5), “moderate” concern (2.6–3.5), and “very” concerned (3.5–5.0).
Additional Measures
We hypothesized that men’s intentions would be influenced by a broad range of factors as posited by the Anderson Model of HealthCare Utilization13,14. This model posits that use of preventive health services vary according to predisposing factors (e.g., demographics, family and social structure, health beliefs, and attitudes), enabling factors (e.g., family and community resources, access to care, insurance), and need factors (e.g., previous illness and individual’s response to illness)14. At visit 43, participants also completed a Men’s Attitude Survey (MAS), which assessed personal attitudes and included 20 statements that assess HAART-related attitudes, safer sex burn-out, and sexual sensation seeking15.
Study Statistics
We used chi-square tests to evaluate differences in categorical variables according to HIV serostatus and study sites. We then used logistic regression analyses to identify independent predictors of intention to seek screening in the next 6 months. The results were similar when intention to seek screening was considered as a binary (data not shown) or categorical outcome, and we present the findings from the categorical outcome here. All variables significant in univariate analysis were included in a multivariate model and removed in a step-wise fashion retaining variables that were statistically significant and those known to be important in the literature, to achieve a final model. All analyses were performed using SAS 9.1.
RESULTS
Men in this analysis were primarily non-Hispanic White (63%) or non-Hispanic Black (26%) and employed full-time (57%) or part-time (11%). Median individual gross income was $35,000 [interquartile range (IQR) = $10,000-“≥$60,000”] and median age was 48 years (IQR = 42–55). Among HIV-infected men, the median CD4 cell count was 728 cells/μl (IQR = 346–701), and the median HIV viral load was undetectable (IQR = undetectable-2313 RNA copies/ml).
Anal Health History and Attitudes
Over a third of participants reported a history of anal warts (Table 1). A history of anal warts was significantly more common in HIV-infected (47%) than HIV-uninfected (32%) MSM (p<0.001). A much smaller proportion of men had anal warts in the past 6 months (3.3%). During semi-annual MACS physical exams, anal warts were directly observed at least once during follow-up in 26% of HIV-positive and 17% of HIV-negative men.
Table 1.
All subjects | HIV-infected | HIV-uninfected | p-value* | ||||
---|---|---|---|---|---|---|---|
N | % | N | % | N | % | ||
Number of men | 1,917 | 901 | 1,016 | ||||
Screening history | |||||||
Ever had anal warts^ | |||||||
No | 1166 | 61% | 479 | 53% | 687 | 68% | <0.0001 |
Yes, but not in the past 6 months | 687 | 36% | 373 | 41% | 314 | 31% | |
Yes, in the past 6 months | 64 | 3.3% | 49 | 5.4% | 15 | 1.5% | |
Ever had anal Pap | |||||||
No | 1,705 | 89% | 759 | 84% | 946 | 93% | <0.0001 |
Yes (all normal) | 178 | 9.3% | 111 | 12% | 67 | 6.6% | |
Yes (≥1 abnormal) | 34 | 1.8% | 31 | 3.4% | 3 | 0.3% | |
Anal Pap in the past 6 months | |||||||
No | 1,821 | 95% | 823 | 91% | 998 | 98% | <0.0001 |
Yes (normal) | 68 | 3.5% | 52 | 5.8% | 16 | 1.6% | |
Yes (abnormal) | 28 | 1.5% | 26 | 2.9% | 2 | 0.2% | |
Attitudes about screening, perceived vulnerability | |||||||
How concerned are you about anal cancer? | |||||||
Not concerned | 1,518 | 79% | 641 | 71% | 877 | 86% | <0.0001 |
Moderately concerned | 231 | 12% | 145 | 16% | 86 | 8.5% | |
Very concerned | 163 | 8.5% | 113 | 13% | 50 | 4.9% | |
How likely are you to be screened for anal cancer or anal warts in the next 6 months? | |||||||
Unlikely | 1,358 | 71% | 545 | 61% | 813 | 80% | <0.0001 |
Possible | 328 | 17% | 190 | 21% | 138 | 14% | |
Likely | 224 | 12% | 164 | 18% | 60 | 5.9% | |
If you suspected an anal health problem where would you go for diagnosis and treatment? | |||||||
Primary physician | 1,462 | 76% | 681 | 76% | 781 | 77% | 0.001 |
STD clinic | 43 | 2.2% | 10 | 1.1% | 33 | 3.2% | |
Gay clinic or health center | 80 | 4.2% | 23 | 2.6% | 57 | 5.6% | |
Anal specialist (proctologist) | 66 | 3.4% | 35 | 3.9% | 31 | 3.1% | |
Dermatologist | 15 | 0.8% | 8 | 0.9% | 7 | 0.7% | |
HIV specialist | 110 | 5.7% | 110 | 12.2% | NA | NA | |
Other | 136 | 7.1% | 32 | 3.6% | 104 | 10.2% | |
Aware of anal cancer screening available in your community | |||||||
No | 980 | 51% | 408 | 45% | 572 | 56% | <0.0001 |
Yes | 932 | 49% | 491 | 54% | 441 | 43% |
*P-values test the difference between HIV-positive and HIV-negative participants for each exposure
^Anal wart exposure based on self-reported history and/or observed presence of anal warts during semi-annual physical exam
Anal Pap screening was relatively uncommon; 89% of this high-risk population reported never having had an anal Pap test (Table 1). HIV-infected men were significantly more likely than HIV-uninfected men to ever have had an anal Pap test (15.7% vs. 6.9%, p<0.001) or an anal Pap in the past 6 months (8.7% vs. 1.8%, p<0.001). Abnormal results were reported by 16% of men who ever had an anal Pap test and 29% of men who had received an anal Pap test in the past 6 months. Among those tested, rates of abnormal anal Pap results were significantly higher in HIV-infected than in HIV-uninfected men for both ever (22% vs. 4.3%, p=0.001) and recent (33% vs. 11%, p=0.06) Pap testing (Table 1).
When participants were asked about their level of concern about anal cancer, more than three-fourths were unconcerned and only 8.5% reported being very concerned (Table 1). HIV-infected men were more likely than HIV-uninfected men to report being very concerned about anal cancer (12.5% vs. 4.9%, p<0.0001). Similarly, the proportion of men reporting likely intention to get anal cancer screening was higher in HIV-infected than HIV-uninfected men (18.2% vs. 5.9%, p<0.001). An additional 17% of MSM reported “possible” intention to seek screening, suggesting screening rates might be increased by motivating these individuals or providing ready access to screening for these men.
Most men (76%) reported they would go to their primary physician if they suspected they had an anal health problem (Table 1), and this proportion was similar in HIV-infected and HIV-uninfected men. Only a small proportion of men said they would go to a STD clinic, HIV specialist, or gay health center for treatment of an anal health problem (Table 1). About half (49%) of men reported they were aware of anal cancer screening available in the community.
Predictors of Intention to Seek Screening
In multivariable analyses, predictors of intention to seek anal cancer screening included predisposing factors, enabling factors, and need factors (Table 2). Predisposing factors associated with an increased intention to screen included Black race (OR = 1.4 95% CI = 1.1–1.9), previous history of anal cancer screening (OR = 1.9 95% CI = 1.4–2.6), having three or more anal receptive sexual partners in the past 6 months (OR = 1.8 95% CI = 1.3–2.4, p-trend = 0.003), and being very concerned about anal cancer (OR = 4.7 95% CI = 3.3–6.7, p-trend<0.001) (Table 2). Attitudes such as safer sex fatigue (OR = 1.3 95% CI = 1.0–1.7) and reduced HIV concern (OR = 1.6 95% CI = 0.98–2.5) were marginally associated with intention to get screened.
Table 2.
Risk factors | N or mean (SD) | OR (95% CI) | |
---|---|---|---|
Univariate | Multivariate* | ||
Demographic factors and screening history (predisposing) | |||
Age (per 5 year increase in age) | 48.3 (10.1) | 0.98 (0.93–1.04) | 1.04 (0.97–1.12) |
Race | |||
White | 1,202 | 1.0 | 1.0 |
Hispanic | 184 | 1.01 (0.72–1.4) | 0.91 (0.59–1.5) |
Black | 504 | 1.72 (1.34–2.1) | 1.42 (1.06–1.9) |
Other | 27 | 0.82 (0.33–2.0) | 0.74 (0.28–2.0) |
City of study recruitment | |||
Baltimore | 371 | 1.0 | 1.0 |
Chicago | 502 | 0.83 (0.63–1.09) | 0.89 (0.66–1.2) |
Pittsburgh | 528 | 0.27 (0.20–0.37) | 0.47 (0.34–0.66) |
Los Angeles | 516 | 0.66 (0.51–0.85) | 0.67 (0.50–0.90) |
Ever have an anal Pap test | |||
No | 1,647 | 1.0 | 1.0 |
Yes | 270 | 4.2 (3.3–5.4) | 1.9 (1.4–2.6) |
Behavioral and attitudinal (predisposing) factors | |||
Anal receptive male sex partners (past 6 months) | |||
0 | 999 | 1.0 | 1.0 |
1–2 | 554 | 1.2 (0.91–1.5) | 1.3 (0.97–1.6) |
≥3 | 364 | 2.0 (1.5–2.6) | 1.8 (1.4–2.5) |
How concerned are you about anal cancer? | |||
Not concerned | 1,523 | 1.0 | 1.0 |
Moderately concerned | 231 | 4.3 (3.3–5.7) | 2.9 (2.2–3.9) |
Very concerned | 163 | 6.5 (4.7–8.8) | 4.7 (3.3–6.7) |
Safer sex fatigue | |||
No | 1,358 | 1.0 | 1.0 |
Yes | 558 | 1.5 (1.2–1.8) | 1.3 (1.0–1.7) |
Perceive HIV as less of a health threat | |||
No | 1,478 | 1.0 | 1.0 |
Yes | 439 | 1.4 (1.1–1.7) | 1.6 (0.98–2.5) |
Enabling factors | |||
Anal cancer screening available in your community | |||
No or unsure | 985 | 1.0 | 1.0 |
Yes | 932 | 3.2 (2.6–4.0) | 2.2 (1.7–2.8) |
Have health insurance | |||
No | 328 | 1.0 | 1.0 |
Yes | 1,589 | 1.6 (1.2–2.1) | 1.9 (1.3–2.6) |
Biological (need) factors | |||
HIV status | |||
HIV uninfected | 1,016 | 1.0 | 1.0 |
HIV infected | 901 | 2.8 (2.3–3.5) | 1.9 (1.5–2.5) |
CD4 (per 100 cell decrease) | 539 (288) | 0.93 (0.85–1.00) | 0.92 (0.84–1.05) |
Log10 viral load, number of HIV RNA copies per mm | 5.6 (2.9) | 0.99 (0.94–1.04) | 1.0 (0.95–1.06) |
Ever have anal warts | |||
No | 1,282 | 1.0 | 1.0 |
Yes | 635 | 1.9 (1.5–2.3) | 1.4 (1.1–1.8) |
*Reported odds ratios (OR) based on a multivariable final logistic regression model adjusted for all other variables in the multivariate column
Enabling factors significantly associated with increased intention to seek screening included awareness of available screening in community (OR = 2.2 95%CI = 1.7–2.8) and current possession of health insurance (OR = 1.9 95% CI = 1.3–2.6). Need-related factors associated with increased intention to seek screening included current HIV infection (OR = 1.9 95% CI = 1.5–2.5) and a history of any anal warts (OR = 1.4 95% CI = 1.1–1.8), especially those with anal warts in the past 6 months (OR = 2.8 95% CI = 1.8–4.4). Among men who were HIV-infected, neither current CD4 count or HIV viral load were significantly associated with intention to seek screening (Table 2). When we conducted similar analyses stratified by HIV status, we found the predictors of intention to seek anal cancer screening to be similar among HIV-infected and HIV-uninfected men (data not shown).
Regional Variability
Intention to seek anal cancer screening varied between MACS study sites. In multivariable analysis, men in Pittsburgh (4.4%) and Los Angeles (12.6%) were significantly less likely to report intention to be screened than men in Baltimore (17.3%) (OR = 0.47, 95% CI = 0.34–0.66 and OR = 0.67, 95% CI = 0.50–0.90, respectively). Men in Chicago (13.5%) reported intermediate rates of intention to screen that were non-significantly different than men in Baltimore (p=0.13) or Los Angeles (p=0.69) and significantly higher than men in Pittsburgh (p<0.001) (Fig. 1). Recent anal screening history was similar in Chicago (7.0%), Baltimore (6.8%), and Los Angeles (5.8%), but significantly lower in Pittsburgh (1.1%, p<0.001). The proportion of men with moderate or high concern about anal cancer was also similar in Chicago (23%), Baltimore (29%), and Los Angeles (24%), and significantly lower in Pittsburgh (9%, p<0.001).
Availability of anal cancer screening, as reported by participants, also varied among cities (Fig. 1). Notably, only half as many participants in Pittsburgh (27%) reported awareness of available community screening as participants in the other MACS cities (51–62%). Intention to seek screening was proportional to the perceived availability of screening in each city (Fig. 1).
DISCUSSION
This study presents recent experiences related to anal cancer prevention in MSM. We found that a relatively small proportion of men had previous experience with anal cancer screening and that a small but clinically significant proportion of these men intend to seek screening in the next 6 months. These rates may be driven by low overall rates of concern about anal cancer among these men. Interest in and use of screening were higher in those MSM at increased risk because of their HIV infection, but even among these men, less than a quarter expressed concern about anal cancer or a stated intention to seek anal cancer screening. We also report that use of anal Pap screening varies substantially among cities and was associated with perceived availability of screening in those communities.
MSM and HIV-infected persons are at increased risk for anal cancer and anal cancer precursors due to a higher prevalence of anal HPV infections due to anal intercourse6,7 and HIV-related immunosuppression16–18. In fact, the rate of anal cancer in these populations (35–100 cases per 100,000 persons) is similar to the rates of cervical cancer before routine cervical cancer screening was introduced5. However, in the absence of clear clinical guidelines for anal cancer screening among MSM, it is unclear whether primary care practitioners should be discussing anal cancer risk or suggesting routine anal Pap testing to MSM. Although mathematical models suggest that routine anal cancer screening of MSM is cost-effective and will improve quality-adjusted life expectancy9, clinical trials have not been completed. Anal cancer screening has good sensitivity among HIV-positive subjects, but the benefits of early treatment have not been well evaluated19. Although relatively few men stated an intention to seek anal cancer screening, the great majority indicated they would go to their primary care physician if they suspected they had an anal health problem. This finding underscores the need for internists and other primary care providers to be able to discuss HPV and anal cancer risk with their patients.
We focused our analysis on intention to seek anal cancer screening to better understand the current needs of this population. In other studies, intention to seek health care is a strong predictor of subsequent use of men’s preventive health services20,21. Screening for other diseases (e.g., mammography, Pap test, and prostate-specific antigen testing) has been associated with both physician recommendations and individual patient factors22–25. Consistent with this and the Anderson Model of HealthCare Utilization14, intention to seek anal cancer screening in this study was related to individual predisposing factors, biological need factors, and community and individual resource enabling factors. The findings from this study thus identify potential barriers to and motivators for anal cancer screening that will need to be addressed if the recommendations to screen for anal cancer become more routine.
The study findings of relatively low rates of anal cancer screening may be a reason for concern among proponents of increased anal cancer screening as many of the men clearly had risk factors, including previous anal warts, sexual risk behaviors, and HIV infection. While HAART has reduced the risk of many HIV-associated morbidities and has dramatically increased survival26, studies suggest that HAART does not decrease risk of HPV-associated (anal, genital, and oropharyngeal) cancers2,16,26,27. Indeed, by providing sufficient time for development of invasive anal disease, longer survival times may lead to continued increases in anal cancer rates in these men. Additional research about the benefits of early detection of anal dysplasias with anal cancer screening is needed to better inform screening recommendations. Another factor to consider is that a vaccine for HPV types 6, 11, 16, and 18, Gardasil, is now licensed for prevention of cervical HPV infections in 9- to 27-year-old females28, and vaccine trials for anal HPV infection in men are currently in progress. However, as Gardasil is a preventive and not a therapeutic vaccine28, it is unlikely that HPV vaccination will be useful in reducing anal cancer incidence in sexually experienced MSM.
Although general attitudinal and psychosocial measures associated with HIV infection were not associated with intention to seek anal cancer screening, concern about anal cancer was strongly associated with increased screening intention. This suggests that if health-care providers discuss anal cancer risk, more individuals may be motivated to seek screening due to increased concern or perceived vulnerability20,21. The fact that enabling factors such as presence of screening programs and ability to pay for screening were strongly associated with intention to seek anal cancer screening underscores that accessible anal cancer screening programs will be important if the goal is to increase rates of screening overall. For example, the regional variation in perceived screening availability closely mirrored intention to screen in those regions. Anecdotally, several investigators involved with the study noted that there does appear to be significant difference in the availability of health-care providers that provide anal cancer screening services, such as an anal Pap smear. Without such expert providers or services, it will be very difficult for men to receive anal cancer screening even if recommended by primary care providers. If anal cancer screening is to become more routine, primary care providers will likely need to play a greater role in the initial screening process.
A few study limitations should be noted. We did not have information on the history of physician discussions with participants regarding anal cancer screening and are unable to distinguish whether lower perceived screening availability reflected actual availability of screening programs in a community. Although the MACS study includes a large number of men from each city, the study participants are unlikely to be representative of all MSM in each city, and thus actual regional rates of anal cancer screening and screening intention in the larger communities might vary from that observed. In addition, screening history and intention to seek screening were collected by self-report and thus may suffer from the potential inaccuracies of all self-reported data. However, the MACS has a long history of collecting valid personal information from its study participants, and sensitive information was obtained via computer rather than face-to-face interview.
In summary, this study provides new information on the current use of anal cancer screening and factors associated with screening in a high-risk sample of men. Although anal cancer is a relatively uncommon cancer in the general population, the incidence among certain populations, such as MSM and HIV-infected individuals, constitutes a considerable risk and may warrant consideration of routine screening29,30. This study suggests that most MSM rely on their primary care physicians for anal health care. Therefore, primary care physicians should be prepared to counsel their patients about the pros and cons of anal cancer screening and be familiar with anal health services in their local communities.
Acknowledgements
Data in this manuscript were collected by the Multicenter AIDS Cohort Study (MACS) with centers (Principal Investigators) at The Johns Hopkins University Bloomberg School of Public Health (Joseph B. Margolick, Lisa Jacobson), Howard Brown Health Center and Northwestern University Medical School (John Phair), University of California, Los Angeles (Roger Detels), and University of Pittsburgh (Charles Rinaldo). The MACS is funded by the National Institute of Allergy and Infectious Diseases, with additional supplemental funding from the National Cancer Institute and the National Heart, Lung and Blood Institute. UO1-AI-35042, 5-MO1-RR-00722 (GCRC), UO1-AI-35043, UO1-AI-37984, UO1-AI-35039, UO1-AI-35040, UO1-AI-37613, UO1-AI-35041. Website located at http://www.statepi.jhsph.edu/macs/macs.html
Conflict of Interest G. D’Souza has consulted for Merck & Co., Inc. R. Cook and D. Wiley have received grant funding from Merck and Co. Inc. D. Wiley has received an honoraria from SCIMED Corp.
References
- 1.Johnson LG, Madeleine MM, Newcomer LM, Schwartz SM, Daling JR. Anal cancer incidence and survival: the surveillance, epidemiology, and end results experience, 1973–2000. Cancer. 2004;101(2):281–288. [DOI] [PubMed]
- 2.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(18):1500–1510. [DOI] [PubMed]
- 3.Hessol NA, Pipkin S, Schwarcz S, Cress RD, Bacchetti P, Scheer S. The impact of highly active antiretroviral therapy on non-AIDS-defining cancers among adults with AIDS. Am J Epidemiol. 2007;165(10):1143–1153. [DOI] [PubMed]
- 4.Goedert JJ, Cote TR, Virgo P, et al. Spectrum of AIDS-associated malignant disorders. Lancet. 1998;351(9119):1833–1839. [DOI] [PubMed]
- 5.Qualters JR, Lee NC, Smith RA, Aubert RE. Breast and cervical cancer surveillance, United States, 1973–1987. MMWR CDC Surveill Summ. 1992;41(2):1–7. [PubMed]
- 6.Chin-Hong PV, Vittinghoff E, Cranston RD, et al. Age-Specific prevalence of anal human papillomavirus infection in HIV-negative sexually active men who have sex with men: the EXPLORE study. J Infect Dis. 2004;190(12):2070–2076. [DOI] [PubMed]
- 7.Daling JR, Madeleine MM, Johnson LG, et al. Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer. Cancer. 2004;101(2):270–280. [DOI] [PubMed]
- 8.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(8):634–641. [DOI] [PubMed]
- 9.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(19):1822–1829. [DOI] [PubMed]
- 10.Pitts MK, Fox C, Willis J, Anderson J. What do gay men know about human papillomavirus? Australian gay men’s knowledge and experience of anal cancer screening and human papillomavirus. Sex Transm Dis. 2007;34(3):170–173. [DOI] [PubMed]
- 11.Kaslow RA, Ostrow DG, Detels R, Phair JP, Polk BF, Rinaldo CR Jr. The Multicenter AIDS Cohort Study: rationale, organization, and selected characteristics of the participants. Am J Epidemiol. 1987;126(2):310–318. [DOI] [PubMed]
- 12.Dudley J, Jin S, Hoover D, Metz S, Thackeray R, Chmiel J. The Multicenter AIDS Cohort Study: retention after 9 1/2 years. Am J Epidemiol. 1995;142(3):323–330. [DOI] [PubMed]
- 13.Anderson JG, Bartkus DE. Choice of medical care: a behavioral model of health and illness behavior. J Health Soc Behav. 1973;14(4):348–362. [DOI] [PubMed]
- 14.Mkanta WN, Uphold CR. Theoretical and methodological issues in conducting research related to health care utilization among individuals with HIV infection. AIDS Patient Care STDS. 2006;20(4):293–303. [DOI] [PubMed]
- 15.Ostrow DG, Silverberg MJ, Cook RL, et al. Prospective Study of Attitudinal and Relationship Predictors of Sexual Risk in the Multicenter AIDS Cohort Study. AIDS Behav 2007. [DOI] [PubMed]
- 16.Palefsky JM, Holly EA, Efirdc JT, et al. Anal intraepithelial neoplasia in the highly active antiretroviral therapy era among HIV-positive men who have sex with men. Aids. 2005;19(13):1407–1414. [DOI] [PubMed]
- 17.Wilkin TJ, Palmer S, Brudney KF, Chiasson MA, Wright TC. Anal intraepithelial neoplasia in heterosexual and homosexual HIV-positive men with access to antiretroviral therapy. J Infect Dis. 2004;190(9):1685–1691. [DOI] [PubMed]
- 18.Holly EA, Ralston ML, Darragh TM, Greenblatt RM, Jay N, Palefsky JM. Prevalence and risk factors for anal squamous intraepithelial lesions in women. J Natl Cancer Inst. 2001;93(11):843–849. [DOI] [PubMed]
- 19.Anderson JS, Vajdic C, Grulich AE. Is screening for anal cancer warranted in homosexual men? Sex Health. 2004;1(3):137–140. [DOI] [PubMed]
- 20.Myers RE, Wolf TA, McKee L, et al. Factors associated with intention to undergo annual prostate cancer screening among African American men in Philadelphia. Cancer. 1996;78(3):471–479. [DOI] [PubMed]
- 21.Kunkel EJ, Meyer B, Daskalakis C, Cocroft J, Jennings-Dozier K, Myers RE. Behaviors used by men to protect themselves against prostate cancer. Cancer Epidemiol Biomarkers Prev. 2004;13(1):78–86. [DOI] [PubMed]
- 22.Montano DE, Taplin SH. A test of an expanded theory of reasoned action to predict mammography participation. Soc Sci Med. 1991;32(6):733–741. [DOI] [PubMed]
- 23.Sheeran P, Orbell S. Using implementation intentions to increase attendance for cervical cancer screening. Health Psychol. 2000;19(3):283–289. [DOI] [PubMed]
- 24.Gattellari M, Young JM, Ward JE. GP and patient predictors of PSA screening in Australian general practice. Fam Pract. 2003;20(3):294–303. [DOI] [PubMed]
- 25.Watson E, Hewitson P, Brett J, et al. Informed decision making and prostate specific antigen (PSA) testing for prostate cancer: a randomised controlled trial exploring the impact of a brief patient decision aid on men’s knowledge, attitudes and intention to be tested. Patient Educ Couns. 2006;63(3):367–379. [DOI] [PubMed]
- 26.International-Collaboration-on-HIV-and-Cancer. Highly active antiretroviral therapy and incidence of cancer in human immunodeficiency virus-infected adults. J Natl Cancer Inst. 2000;92(22):1823–1830. [DOI] [PubMed]
- 27.Biggar RJ, Chaturvedi AK, Goedert JJ, Engels EA. AIDS-related cancer and severity of immunosuppression in persons with AIDS. J Natl Cancer Inst. 2007;99(12):962–972. [DOI] [PubMed]
- 28.Garland SM, Hernandez-Avila M, Wheeler CM, et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med. 2007;356(19):1928–1943. [DOI] [PubMed]
- 29.Daling JR, Weiss NS, Hislop TG, et al. Sexual practices, sexually transmitted diseases, and the incidence of anal cancer. N Engl J Med. 1987;317(16):973–977. [DOI] [PubMed]
- 30.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(9):1127–1134 [DOI] [PubMed]