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Clinical Science

Racial Disparities in Anal Cancer Screening Among Men Living With HIV: Findings From a Clinical Cohort Study

Gillis, Jennifer L. MSca,b,c; Grennan, Troy MDd,e; Grewal, Ramandip MPHa,c; Ogilvie, Gina MDd,e; Gaspar, Mark PhDa; Grace, Daniel PhDa; Lofters, Aisha MDa,c,f; Raboud, Janet M. PhDa,b; Saarela, Olli PhDa; Rosenes, Ron LLDb; Salit, Irving E. MDb; Burchell, Ann N. PhDa,c,g; the OHTN Cohort Study Team

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: July 1, 2020 - Volume 84 - Issue 3 - p 295-303
doi: 10.1097/QAI.0000000000002335
  • Free

Abstract

INTRODUCTION

Similar to other high-resource countries, people living with HIV in Canada are aging due to advancement in the treatment of HIV and health care.1 As with all aging populations, cancer is a significant health concern and cancer is the most common cause of death among people living with HIV.2,3 Individuals living with HIV are at higher risk of most cancers than their HIV-negative counterparts,4–8 specifically cancers with known infectious causes such as human papillomavirus (HPV)-associated anal cancer, one of the most common non–AIDS-defining cancers.4,9 In North America, men living with HIV are up to 100 times more likely to get anal cancer than the general male population,10,11 with incidence rates of anal cancer estimated between 45 and 131 per 100,000 compared with 1–2 per 100,000 individuals in the HIV-negative population.10–14 To reduce this burden, anal cytology (Papanicolau, or “Pap” test) can be used to screen for anal precancerous changes.15 High resolution anoscopy (HRA) with directed biopsies is used to confirm the presence of anal cancer precursor lesions of the anal canal.16,17 Digital anal rectal examinations (DARE) can be used to identify anal cancers especially if anal cytology and HRA are unavailable18; this modality is also used for other health checks (eg, prostate screening).18

In Canada, access to anal cytology and HRA screening modalities is presently limited and concentrated in large, urban centres.18 Although research studies evaluating these anal cancer screening modalities have assessed acceptability,19–22 few studies have quantified real-world uptake or examined disparities in screening that highlight potential barriers to implementation of screening programs or guidelines.22–25 Disparities in cancer screening and outcomes by race, immigration status, and socioeconomic factors, among others, have been identified for cervical, breast, and colorectal cancer for which there are formalized screening programs, as well as prostate cancer for which screening guidelines are evolving.26–30 The identification of these disparities points to a larger issue regarding health equity, particularly for population subgroups for whom social factors, including race and racism, significantly impact health outcomes.31–33 Disparities in anal cancer and related outcomes such as anal HPV infection and dysplasia have been identified in the literature.34 Therefore, additional research is needed to identify factors associated with anal cancer screening uptake in general HIV clinical practice and to examine the broader impact of these factors when considering development of screening guidelines or programs and their implementation.

As noted, few studies have quantified the prevalence of anal cancer screening within a population at particularly high risk for HPV-associated anal cancer, such as men living with HIV. We conducted this study to determine the proportion of men who have undergone anal cancer screening and examined factors associated with having ever been screened in a cohort of men living with HIV attending HIV specialty care clinics in Ontario, Canada. We hypothesized that more men who identify as gay, bisexual, and other men who have sex with men will have been screened compared with heterosexual men and that there may have been disparities in screening by race.

METHODS

Study Participants

A quantitative questionnaire module examining HPV, its associated diseases, and their prevention was administered to active male participants of the Ontario HIV Treatment Network Cohort Study (OCS). The OCS is a volunteer-based cohort of people living with HIV attending one of 9 HIV specialty care clinics in Ontario, Canada.35 Individuals are eligible for inclusion in the OCS if they have laboratory documented HIV infection, have the ability to provide informed consent, and are 16 years or older. Since 1996, more than 6500 participants have been enrolled in the cohort and approximately 2900 men are currently under active follow-up, completing annual interviewer-led questionnaires. These annual interviews collect rich sociodemographic, behavioral, and psychosocial measures. In addition, clinical charts are abstracted every 6 months, collecting information on CD4 count, viral load, and comorbidities.

HPV Module and Key Data Elements

The HPV questionnaire module, included in the 2016–2017 annual OCS interviews, was developed based on questionnaires used in previous research on HPV, its associated diseases, and their prevention.36–46 The Theory of Planned Behaviour40,42,47,48 guided the development of questions examining beliefs regarding HPV-associated disease prevention. Where possible, questions used in previous studies were chosen to facilitate comparison of results. This quantitative questionnaire module was developed as part of the HPV-Screening and Vaccine Evaluation (HPV-SAVE) study,49,50 which aims to gain insight into how to best deliver anal cancer screening, treatment, and vaccination programs for men living with HIV who are at particularly high risk of HPV-associated anal cancer, specifically gay, bisexual, and other men who have sex with men. This module was designed to capture the patient perspective, aiming to assess men's knowledge and attitudes regarding HPV, anal cancer, and associated prevention strategies. To be eligible for this HPV questionnaire module, OCS participants had to self-identify as male (cis- or trans-; self-identified female participants completed a separate set of questions, with findings to be reported in a future publication). Within this module, men were asked a series of questions to assess their lifetime experience with anal cancer screening including digital anal rectal examination (DARE), anal Pap cytology, and anoscopy. Relevant questions are presented in Table 1. Sexual orientation and race were self-identified by participants and recorded by interviewers using prespecified categories with an option to specify response (Table 1). Men were able to identify as multiple races. Race was categorized as Indigenous; African, Caribbean, or black; Asian; white; Latin American; and multiple races.

T1
TABLE 1.:
Summary of Relevant Questions From the OCS Questionnaire Administered to Men Attending HIV Specialty Clinics in Ontario, Canada, in 2016–2017

Statistical Methods

Logistic regression was used to identify factors associated with the following self-reported outcomes: (1) having ever discussed anal cancer screening with a health professional, (2) having ever had DARE, and (3) having ever undergone anal cytology or anoscopy (a composite outcome). For the third, we opted for a composite outcome, as not all sites and consequently men have access to trained anoscopists. We conducted a sensitivity analysis for this composite outcome by restricting to the subset of clinic sites that have on-site HRA capabilities or easily accessible referrals (ie, in same city) and stratifying on site. For all outcomes, a staged modeling approach was used to evaluate the hypothesis that experience with anal cancer screening differs by sexual orientation and race. Multivariable models for each outcome were developed by first examining the association of race and sexual orientation, adjusting for continuous age (centered at the median) as a common confounder. Years since HIV diagnosis, as proxy for contact with health care, and self-reported previous diagnosis with AIDS, as proxy for depth of immunosuppression, were included in subsequent models. For models examining past screening with DARE and cytology/anoscopy, men's comfort discussing anal health and knowing someone with HPV-associated cancer were included. Finally, education and income were included to examine their impact on any potential racial disparities in screening. Results from the final models are reported as adjusted odds ratios (aORs) with 95% confidence intervals (CIs). All analyses were conducted using SAS 9.4 (SAS Institute, Inc., Cary, NC).

Research Ethics Approval

The HPV questionnaire module was approved by the HPV-SAVE Community Advisory Committee and the OCS Governance Committee. Research ethics approval was received from the research ethics boards of all participating OCS sites, St. Michael's Hospital, University Health Network, and University of Toronto.

RESULTS

In total, 1677 men had a scheduled clinic visit and completed the OCS questionnaire during the period when the HPV module was active (April 2016–June 2017). This represents 58% of the 2893 men under active follow-up in the OCS. Over 99% of men who completed the questionnaire self-identified as cisgender. Seventy-two percent (72%) self-identified as gay, 7% as bisexual, 5% as other men who have sex with men, and 16% as heterosexual. As outlined in Table 2, the median age (interquartile range) was 53 (45–59) and 70% of men identified as white, 11% African, Caribbean, or black (ACB), 7% Asian, 5% Latin American, 4% Indigenous, and 4% as multiple races. In total, 28% of men reported ever being told by a health care provider that they had anogenital warts, 14% HPV, and 7% anal precancer.

T2
TABLE 2.:
Characteristics of Men Living With HIV Who Completed the Human Papillomavirus (HPV) Questionnaire Module in 2016–2017 in the OCS in Canada.

More than 85% of men indicated they are comfortable or very comfortable discussing their anal health with their HIV or family doctor and 38% reported having discussed anal cancer screening with a health care provider. The majority of these men (87%) indicated that it was the health care provider who initiated the discussion. Among men who identified as gay, bisexual, or other men who have sex with men, half (50%) of men aged 50 years or older reported having discussed anal cancer screening with a health care provider compared with 32% of younger men. Among men who identified as heterosexual, only 17% of those over 50 years old and 5% under age 50 reported having discussed anal cancer screening with a health care provider. In the multivariable logistic regression model (Table 3), gay men (aOR = 5.27; 95% CI: 3.60 to 7.72), bisexual men (aOR = 2.51; 95% CI: 1.49 to 4.23), and other men who have sex with men (aOR = 3.30 95% CI: 1.65 to 6.60) were more likely than heterosexual men to have discussed screening. After adjusting for sexual orientation and age, Asian men (aOR = 0.48; 95% CI: 0.29 to 0.80) were less likely than white men to have previously discussed anal cancer screening with a health care provider. Even when restricting the analysis to gay, bisexual, and other men who have sex with men, Asian men (aOR = 0.57; 95% CI: 0.34 to 0.94) were less likely than white men to have discussed screening.

T3
TABLE 3.:
Factors Associated With Having Discussed Anal Cancer Screening With a Health Care Provider Among Men Living With HIV Attending HIV Specialty Clinics in Ontario, Canada, in 2016–2017

The majority of men (70%) reported ever having had DARE with the majority reporting having had DARE within the past 3 years (75%). In the logistic regression model examining experience with DARE and adjusting for sexual orientation, age, education, and income (Table 4), men who identified as African, Caribbean, or black (aOR = 0.47; 95% CI: 0.31 to 0.70) or Asian (aOR = 0.27; 95% CI: 0.17 to 0.44) were less likely to have had DARE than white men. Conversely, time since HIV diagnosis was positively associated with having had DARE, with those diagnosed longer ago were more likely to have had the examination (for every 5 years since HIV diagnosis, aOR = 1.16; 95% CI: 1.06 to 1.27). Men who have known someone with HPV-associated cancer (aOR = 1.81; 95% CI: 1.15 to 2.86) and those comfortable discussing anal health with their family doctor (aOR = 1.65; 95% CI: 1.18 to 2.29) were also more likely to have had DARE. Inference remained the same when restricting the analysis to gay, bisexual, and other men who have sex with men.

T4
TABLE 4.:
Factors Associated With Lifetime Experience With Digital Anal Rectal Examinations (DARE) Among Men Living With HIV Attending HIV Specialty Clinics in Ontario, Canada, in 2016–2017

Overall, 40% of men reported having ever been screened for anal cancer by either anal cytology or anoscopy with the majority screened within the past 3 years (81%). As shown in Table 5, the proportion of men screened by anal cytology or anoscopy ranged from 48% among gay men to 12% among heterosexual men. In the multivariable regression model accounting for sexual orientation, age, education, and income, Asian men (aOR = 0.51; 95% CI: 0.31 to 0.83) were less likely than white men to have undergone anal cytology or anoscopy. These findings remained when restricting the analysis to gay, bisexual, and other men who have sex with men (Table 5). Those diagnosed with HIV longer ago (per 5 years since HIV diagnosis, aOR = 1.09; 95% CI: 1.01 to 1.18) were more likely to have had cytology or anoscopy, as observed for DARE. Results were consistent in a sensitivity analysis conducted among clinics with on-site or accessible referral capabilities for HRA, which captured 84% of men (n = 1410 of 1677) (data not shown).

T5
TABLE 5.:
Factors Associated With Lifetime Experience With Anal Cytology or Anoscopy for Anal Cancer Screening Among Men Living With HIV Attending HIV Specialty Clinics in Ontario, Canada, in 2016–2017

DISCUSSION

In this sample of 1677 men living with HIV attending HIV specialty clinics in a single-payer health care setting in Ontario, Canada, 40% of men reported having been screened for anal cancer by anal cytology or anoscopy and 70% of men reported having had DARE. As anticipated, men who identified as gay, bisexual, or other sexual minorities were more likely than heterosexual men to have discussed anal cancer screening and to have been screened. After accounting for differences in sexual orientation and age, that may influence provider recommendations for anal cancer screening, the proportion of men screened differed by self-identified race. Compared with white men, Asian men were less likely to have discussed screening with a health care professional as well as less likely to have been screened by any modality, and men who identified as African, Caribbean, or black were less likely to have had DARE. These disparities were still observed when restricting the analyses to men considered at particularly high risk of anal cancer—gay, bisexual, and other men who have sex with men.

Our results are largely consistent with the few studies that have assessed prevalence of anal cancer screening outside of formalized research studies that have specifically recruited men for screening. In a study among men who have sex with men in the United States, 74% of men reported having undergone DARE, anal cytology, or both.24 HIV-negative men were less likely to have had either procedure, as were black men (aOR = 0.20; 95% CI: 0.10 to 0.5) and younger men.24 The Anal Health Study, nested within the Multicenter AIDS Cohort Study in the United States, quantified the prevalence of past screening by anal cytology among participants, finding only 23% of men had been previously been screened for anal cancer before entering the study.22 This increased to 39% among men living with HIV.22 The authors did not evaluate factors associated with past screening, although they found that acceptance of the offer of free screening within their study differed by race with identifying as black (OR = 2.15; 95% CI: 1.18 to 3.90) being associated with refusing screening after adjusting for age, city of clinic, income, and education.22 The results of our study are also largely consistent with the literature on other screen-preventable cancers, wherein disparities in screening and outcomes have been identified.26–30 Moreover, a systematic review of studies conducted in the United States identified potential racial disparities in anal cancer and related outcomes.34 However, the authors of this review specifically noted an underrepresentation of black men who have sex with men in such studies and were unable to comment on disparities in clinical care and corresponding impact on clinical outcomes.34

We acknowledge that race is a social construct and proxy for a multitude of factors that impact access to and engagement in clinical care for racialized men. The complexity of these individual-, provider-, and systems-level factors cannot be overstated. For instance, individual-level factors, such as engagement in and perceptions of care, intersect with provider-level factors that include counseling patients about anal cancer and offering appropriate screening. All of these factors are influenced by social context and systems-level factors such as institutional emphasis on and training for culturally competent and antiracist care.31,51,52 Owing to the cross-sectional nature of this questionnaire module, it is difficult to disentangle how these factors contribute to disparities in anal cancer screening. However, it is imperative that disparities in cancer screening are measured to identify and ultimately rectify inequities in health care delivery and participation,31,53 particularly as guidelines are developed and implemented to improve anal cancer screening and reduce the burden of anal cancer among men living with HIV.

In conjunction with emerging literature, our results suggest future areas of inquiry to elucidate barriers and facilitators to participation in anal cancer prevention strategies. Specifically in qualitative studies among gay, bisexual, and other men who have sex with men, health care provider recommendation has been identified as a leading facilitator to screening,54–56 which has also been observed for breast, cervical, and colorectal cancer screening.57Men in our study indicated that discussions regarding screening were predominantly initiated by a health care provider. However, because of a lack of endorsed guidelines for anal cancer screening, provider recommendations and patient counseling are particularly complex. At present, both physicians and patients need to navigate significant uncertainty around the benefits of screening and treatment of anal precancer when determining what is best for the individual. For providers, this may mean balancing capacity concerns, diagnostic ambiguity, and patient anxieties when recommending and conducting anal cancer screening.58 For patients, this often means understanding and accepting anal cancer as a significant comorbidity risk in the context of living with HIV.50,54,55 This process is further complicated by perceptions about racialized men's sexuality and consequently anal cancer risk, which inform how clinical encounters unfold between provider and patient.54 Future work should develop and evaluate strategies that address how and to whom providers offer screening, thereby supporting effective and respectful provider–patient communication to help individuals navigate the complex decision-making process.57,58

Our work is limited by the use of a self-reported measure for past anal cancer screening in a cross-sectional study. The procedures for DARE, anal cytology, and anoscopy were described in the questionnaire to aid men's recollection. However, there is still the potential for men to have mistaken anal Pap tests for anal cultures and anoscopy for other endoscopic methods (eg, sigmoidoscopy and colonoscopy), and DARE may have been performed for other health purposes. We are planning studies to validate these self-reported measures using chart and laboratory data. Gay, bisexual, and other men who have sex with men attending OCS clinical sites in Toronto, Ontario, may have had access to anal cytology and anoscopy through local research studies.37,59 Moreover, this questionnaire was administered to men in a volunteer cohort of people living with HIV engaged in HIV specialty care. Altogether, our study may overestimate the proportion of men living with HIV who have had DARE, anal cytology, or anoscopy for anal cancer screening. HRA is a limited resource at present such that some clinic sites did not have access to trained anoscopists, producing interclinic variability that might have biased the assessment of correlates of screening. However, a subset analysis stratified by site and restricted to men from clinic sites with access to anoscopy was consistent with the presented findings. A significant strength of this work is the use of this large sample of men living with HIV. To the best of our knowledge, this is the largest study to-date that has examined self-reported receipt of anal cancer screening. Even as one of the largest studies to-date, our analysis is limited in its use of broad categories of race, as some distinct ethnoracial groups had to be combined (eg, South Asian and East Asian) due to sample size considerations. Our study was not restricted only to men who have identified as having had sex with men, and it assessed receipt of screening beyond that available only through research studies. Furthermore, focusing on men receiving HIV specialty care allowed us to first assess disparities in anal cancer screening among a group of men amenable to increased engagement in preventive medicine strategies. Most men in this study were comfortable discussing their anal health with their HIV specialist or family doctor. This offers an avenue of engagement to increase anal cancer screening among men at particularly high risk of anal cancer.

Uncertainty remains regarding the optimal use of anal cytology or anoscopy as a means to reduce the burden of anal cancer among men living with HIV. At present, these screening procedures are relegated to research studies or available only at select centers concentrated in large, urban areas in Canada.60 Such issues may be reflected in the disparities observed and low proportion of men already engaged in clinical care who had undergone these procedures, even among the gay, bisexual, and other men who have sex with men in our study. However, disparities were still observed in receipt of DARE, an established procedure for which physicians are readily trained. As evidence is amassed to address uncertainty around anal cancer screening, strategies that encourage effective provider–patient communication and equitable recommendations for screening should be carefully considered. As such, future research should identify and examine meditating factors (eg, engagement in and positive perceptions of care; provider–patient communication regarding screening; institutional policies regarding culturally competent care) to provide additional insight into how to best deliver anal cancer screening in men living with HIV. Ultimately, health equity should be a cornerstone in the development of anal cancer screening guidelines or programs, with health equity impact assessments planned to ensure equitable implementation across axes of HIV serostatus, sexual orientation, ethnoracial identity, and socioeconomic status, among other facets of men's lives.61

CONCLUSIONS

Our findings highlight the potential for disparities in anal cancer screening that need to be considered when developing guidelines and screening programs to reduce the burden of anal cancer among men living with HIV and ensure health equity.

ACKNOWLEDGMENTS

The authors gratefully acknowledge all the people living with HIV who volunteered to participate in the OHTN Cohort Study and the work and support of the past and present members of the OCS Governance Committee: Barry Adam, Adrian Betts, Anita C. Benoit, Breklyn Bertozzi, Les Bowman, Alison Bray, Lisungu Chieza, Desmond Chuang, Tracey Conway, Jasmine Cotnam, Patrick Cupido, Tony Di Pede, Brian Finch, Esther Guzha, Muluba Habanyama, Michael J. Hamilton, Brian Huskins, Rick Kennedy, Julia Kimmaliardjuk, Ken King, Nathan Lachowsky, Joanne Lindsay, Shari Margolese, John MacTavish, Mark McCallum, Martin McIntosh, Mary Ndung'u, Sam Ocen, Colleen Price, Rodney Rousseau, Viviana Santibañez, Lori Stoltz, Darien Taylor, Rosie Thein, and Drs. Ahmed Bayoumi, Evan Collins, Curtis Cooper, Clemon George, T.G., Claire Kendall, Greg Robinson, and Alan Li. The authors acknowledge the current members of the Scientific Steering Committee: Dr. Barry Adam, Dr. Anita Benoit, Adrian Betts, Dr. David Brennan, A.N.B., Tracey Conway, Dr. Curtis Cooper, Pierre Giguere, Dr. Trevor Hart, Dr. Winston Husbands, Dr. Abigail Kroch, Lucia Light, Dr. Mona Loufty, Dr. Lawrence Mbuagbaw, Wesley Oakes, Dr. Kelly O'Brien, and Dr. Sergio Rueda.

The authors thank all the interviewers, data collectors, research associates and coordinators, nurses, and physicians who provide support for data collection and extraction. The authors wish to thank the OCS staff for data management, IT support, and study coordination: Eliot Winkler, Wesley Oakes, Lucia Light, Veronika Moravan, Nahid Qureshi, Tsegaye Bekele, Sean Colyer, Maya Kesler, and Kristen O'Brien. The OHTN Cohort Study is supported by the Ontario Ministry of Health and Long-Term Care.

The HPV-SAVE (HPV Screening and Vaccine Evaluation) Team includes I.E.S., T.G., R.R., Jason Brunetta, Owen McEwen, Ann Burchell, Rupert Kaul, Paul MacPherson, Janet Raboud, Anita Rachlis, Alberto Severini, Darrell Tan, Jill Tinmouth, Daniel Grace, and Joel Palefsky. The authors acknowledge the contribution of the HPV-SAVE Community Advisory Committee (R.R., Robert Reinhard, Evan Collins, Len Tooley, Owen McEwen, David McLay, Llewelyn Goddard, and Jordan Prosper).

The OHTN Cohort Study Team consists of Dr. Abigail Kroch (Principal Investigator), University of Toronto, PHO and OHTN; Dr. Ann Burchell, St. Michael's Hospital; Dr. Sergio Rueda, CAMH; Dr. Gordon Arbess, St. Michael's Hospital; Dr. Jeffrey Cohen, Windsor Regional Hospital; Dr. Curtis Cooper, Ottawa General Hospital; Elizabeth Lavoie, University of Ottawa Health Services; Dr. Fred Crouzat, Maple Leaf Medical Clinic; Dr. Nisha Andany, Sunnybrook Health Sciences Centre; Dr. Sharon Walmsley, Toronto General Hospital; Dr. Michael Silverman, St. Joseph's Health Care; Dr. Roger Sandre, Sudbury Regional Hospital; Wangari Tharao, Women's Health in Women's Hands Community Health Centre; Holly Gauvin, Elevate NWO; and Dr. Fiona Smaill, Hamilton Health Sciences Centre.

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Keywords:

anus neoplasms; human papillomavirus; early detection of cancer; anoscopy; anal cytology; HIV; racial disparities

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