Abstract
Without standard guidelines, there is a critical need to examine anal cancer screening uptake in the South which has the highest HIV incidence in the U.S. We identified factors associated with screening among men living with HIV (MLHIV) at a large academic HIV outpatient clinic in Alabama. Relationships between sociodemographic, clinical, sexual risk characteristics and screening were examined using T-tests, Fisher’s exact, Chi-square, and logistic regression analyses. Unadjusted and adjusted odds ratios (AOR) were computed to estimate the odds of screening.
Among 1,114 men, 52% had received annual anal cytology (pap) screening. Men who were screened were more likely to have multiple sexual partners compared to men who were not screened (22.8% vs. 14.8%, p=0.002). Among men with one partner, the youngest were almost five times more likely to be screened compared to middle-aged men (AOR=4.93, 95% CI: 2.34–10.39). Heterosexual men had lower odds and men who reported unprotected anal sex had higher odds of screening. Our findings suggest a racial disparity, with older black MLHIV being the least likely to be screened. In the South, MLHIV who are older, black, heterosexual, or live in high social vulnerability counties may be less likely to receive annual anal cancer screening.
Keywords: anal cancer screening, HIV, sexual risk characteristics, social vulnerability, Deep South
Introduction
Anal cancer incidence has been increasing worldwide in recent years, with an estimated 50,865 new cases, and causing an estimated 19,293 deaths in 2020 (Sung et al., 2021). In the U.S., there will be an estimated 9,760 new cases and 1,870 deaths caused by anal cancer in 2023 (SEER, 2023). Anal squamous cell carcinoma is almost exclusively (>90%) caused by persistent human papillomavirus (HPV) high risk types (NCI, 2022). Several groups are at higher risk of anal cancer, including people living with HIV (PLHIV), men who have sex with men (MSM), women with HPV-associated precancer and cancers of the cervix, vulva, and vagina, solid organ transplant recipients, and people with certain autoimmune diseases (Clifford et al., 2021; Colón-López et al., 2018). Recent studies indicate that the incidence rate of anal cancer among MSM living with HIV is between an estimated 85-131 cases per 100,000 person-years compared to an estimated 1.9 cases per 100,000 person-years in the general population (Clifford et al., 2021; Colón-López et al., 2018; SEER, 2023).
Black MSM have the highest rates of HIV infection in the U.S. (CDC, 2020). In both the general population and among PLHIV, black men have a worse prognosis for anal cancer (Arora et al., 2017; Bojko et al., 2018). Black men are more likely to be diagnosed at an earlier age and at a later stage of disease, and face poorer survival (Bojko et al., 2018). Deshmukh et al. reported that younger black men born during the 1980’s had an estimated five-times higher risk of anal cancer compared to older men born during the 1940’s (Deshmukh et al., 2020). Furthermore, there is evidence to suggest that black men are more likely to decline screening compared to men from other racial backgrounds (D’Souza et al., 2013; Kreuter et al., 2010; Newman et al., 2008). A recent study conducted in Texas found that black MSM were 80% less likely to report a history of screening compared to white MSM (Hicks et al., 2019).
The Southern region of the U.S. continues to have the highest incidence rate of HIV infection, accounting for 52% of new infections diagnosed in the U.S. in 2021 (CDC, 2023). In the South, black men and women are disproportionately affected by HIV, accounting for 52% of new infections in 2020 (CDC, 2022). Early detection of precancerous lesions can prevent morbidity related to treatment and mortality caused by anal cancer; however, uptake and barriers to screening have not been fully explored. There may be unique barriers in the South, particularly in rural settings, including lack of access to care or transportation barriers. The CDC’s Agency for Toxic Substances and Disease Registry’s Social Vulnerability Index (SVI) can be utilized to assess the impact of such structural barriers, like poverty, which may be prevalent in the South. The impact of social vulnerability, defined as “the potential negative effects on communities caused by external stresses on human health,” on anal cancer screening, is largely unknown in this population (ATSDR, 2022).
Currently, anal cancer screening guidelines are lacking in the U.S. which likely has led to delayed detection and missed opportunities for prevention of anal cancer (Chiu et al., 2015; Kang et al., 2018; Nelson et al., 2013; J. S. Wells et al., 2014; Ye et al., 2021). Annual screening by digital rectal exams (DRE) or anal cytology (pap) tests among PLHIV starting at the age of 35 years of age, independent of HPV-vaccination status and cervical disease history is recommended by some experts (Hirsch et al., 2022). Recently published findings from the Anal Cancer/HSIL Outcomes Research (ANCHOR) study, a large, phase 3 trial, provide strong evidence that treatment of anal high-grade squamous intraepithelial lesions (HSIL) is effective in reducing the incidence of anal cancer (Palefsky et al., 2022). It is expected that results of this study will lead to updates in federal guidelines on anal cancer screening in the U.S. soon. Given the substantial burden of HIV in the South and recent upward trends of HPV-associated cancers among younger people globally, it is important to identify barriers to anal cancer screening among PLHIV in this region (Kang et al., 2018; Young et al., 2015). In the current study, we aimed to do identify factors associated with and barriers to screening among MLHIV at a large academic HIV outpatient clinic in Alabama.
Methods
Study population
The current study examined sociodemographic, clinical, and sexual risk characteristics associated with anal cancer screening among MLHIV who receive HIV care at an outpatient clinic at the University of Alabama at Birmingham (1917 Clinic). The 1917 Clinic is the largest HIV specialty care clinic in Alabama; it has served more than 6,000 PLHIV in the Southeast since opening in the 1980’s (UAB, 2023). We examined recent trends in anal cancer screening uptake among men who received care from the clinic in 2018.
Data sources
Sociodemographic and clinical data were abstracted from medical charts; patient reported outcomes (PRO) were collected previously using the UAB Center for AIDS Research Network of Integrated Clinical Systems (CNICS) PRO Questionnaire, which is routinely self-administered among patients every 4 to 6 months (Kitahata et al., 2008; Mimiaga et al., 2015; Satyanarayana et al., 2021). Data from men who completed the sexual risk questions on the questionnaire in 2018 were retrospectively abstracted for analyses. UAB Institutional Review Board approval was obtained for all research procedures (Record number IRB-300006759). We utilized existing de-identified data and informed consent was waived by the IRB.
Outcome and predictor variables
The outcome of the study was screening (i.e., anal cytology pap) within one year of completing the questionnaire. At the clinic, anal cytology pap testing is offered annually, particularly for those patients who report a history of receptive anal sex as a primary risk factor. Additional risk factors, such as a history of abnormal pap test results, may indicate more frequent pap testing for certain patients. The predictor variables included sociodemographic, clinical, and sexual risk characteristics. Sociodemographic characteristics included age, race, sexual identity, and county-level SVI. The CDC’s SVI considers the following factors: housing and transportation, socioeconomic status, proportion of racial and ethnic minorities, and household characteristics. SVI ranges from 0 to 1, with 1 indicating the highest vulnerability. We used quartiles to categorize SVI, including lowest vulnerability (≤0.2500), low to moderate vulnerability (0.2501-0.5000), moderate to high vulnerability (0.5001-0.7500), and highest vulnerability (≥0.7501).
Clinical data included years treated at the clinic, body mass index (BMI; kg/m2), viral load (VL; copies/mL), and CD4 count (cells/mm3) at the time of questionnaire completion or the most recently collected sample (within one year of taking the questionnaire). Self-reported data included antiretroviral (ARV) use and sexual risk characteristics. Patient-reported sexual risk characteristics are based on the preceding three months of the questionnaire, and include number of sexual partner(s), gender and HIV status of partner(s), HIV medication and pre-exposure prophylaxis (PrEP) use of partner(s), participation in unprotected vaginal, anal, and oral sex, and patient concern of recent STI exposure or HIV re-exposure.
Statistical analyses
Bivariate analyses included T-tests and Fisher’s exact tests for continuous variables and Chi-square tests for categorical variables and examined potential associations with screening uptake and predictor variables. An alpha threshold of p<0.05 was used to define statistical association. Odds ratios to estimate screening were computed using multivariable logistic regression models. Men who reported two or more partners within the previous three months of questionnaire completion were more likely to receive screening; therefore, multivariable analyses were conducted separately by the number of partners (1 vs. 2 or more). Men who reported zero partners in the preceding three months did not complete the sexual risk characteristic questions of the questionnaire as they concern information about current partner(s) and current sexual practices. Thus, men with zero partners were not included in the multivariable analyses.
Factors statistically associated with screening in bivariate analyses were included in the multivariable models. To avoid multicollinearity and spurious associations, the following predictors were not included in the adjusted models: self-reported ARV use and CD4 Count. As a separate sensitivity analysis, an additional adjusted model that included all participants (independent of the number of sexual partners) was computed, and no differences were seen. Additional stratified analyses (T-tests, Fisher’s exact tests, and Chi-square tests) examined screening associations by age, race, and SVI.
Results
Sociodemographic characteristics, clinical characteristics, and screening uptake
Among 1,159 men who completed the CNICS questionnaire in 2018, 31 men who did not reside in Alabama and 14 men who had a history of anal cancer were excluded, leaving a final sample of 1,114 men included in the analyses (Figure 1). Half (52%) had received anal cytology (pap) screening within one year (Table 1). Ages ranged from 20 to 79 years, with a median of 48 years. About 55% of the men were black and 43% were white. The majority of men (~80%) resided in AL counties with moderate to high social vulnerability. Years treated at the clinic ranged from about 4 ½ months to 27 years and did not significantly differ between men screened and men who were not. Almost all (~96%) self-reported ARV use and about 92% had undetectable VL (<200 copies/mL).
Figure 1.
Participant Exclusion Flow Diagram
Table 1.
Sociodemographic and clinical characteristics by anal cancer screening uptake within one year of completing the CNICS PRO* questionnaire
| Total Sample N=1114 N(%) |
Screened N=580 N(%) |
Not screened N=534 N(%) |
p-value** | |
|---|---|---|---|---|
| Age, years, median (Q1, Q3) | 48 (35,55) | 45 (32,54) | 50 (40,57) | <0.001 |
| Age, years, range | 20-79 | 20-71 | 20-79 | |
| Age group, years | <0.001 | |||
| 20-34 | 255 (22.9) | 181 (31.2) | 74 (13.9) | |
| 35-44 | 211 (18.9) | 105 (18.1) | 106 (19.9) | |
| 45-54 | 333 (29.9) | 160 (27.6) | 173 (32.4) | |
| 55-64 | 256 (23.0) | 119 (20.5) | 137 (25.7) | |
| ≥65 | 59 (5.3) | 15 (2.6) | 44 (8.2) | |
| Race | 0.007 | |||
| Black | 615 (55.2) | 297 (51.2) | 318 (59.8) | |
| White | 476 (42.8) | 274 (47.2) | 202 (38.0) | |
| Other*** | 21 (1.9) | 9 (1.6) | 12 (2.3) | |
| Sexual identity (N=672) | <0.001 | |||
| Homosexual | 414 (61.6) | 267 (76.7) | 147 (45.4) | |
| Heterosexual | 141 (21.0) | 11 (3.2) | 130 (40.2) | |
| Bisexual | 76 (11.3) | 50 (14.4) | 26 (8.0) | |
| Other | 41 (6.1) | 20 (5.8) | 21 (6.5) | |
| County Social Vulnerability ± | 0.072 | |||
| Lowest vulnerability (≤0.2500) | 68 (6.1) | 43 (7.4) | 25 (4.7) | |
| Low to moderate vulnerability (0.2501-0.5000) | 59 (5.3) | 29 (5.0) | 30 (5.6) | |
| Moderate to high vulnerability (0.5001-0.7500) | 887 (79.6) | 448 (77.2) | 439 (82.2) | |
| Highest vulnerability (≥0.7501) | 100 (9.0) | 60 (10.3) | 40 (7.5) | |
| BMI, kg/m2 | 0.087 | |||
| Underweight (<18.5) | 37 (3.3) | 17 (2.9) | 20 (3.8) | |
| Average weight (18.5-24.9) | 419 (37.6) | 237 (40.9) | 182 (34.1) | |
| Overweight (25.0-29.9) | 367 (32.9) | 188 (32.4) | 179 (33.5) | |
| Obese (≥30.0) | 291 (26.1) | 138 (23.8) | 153 (28.7) | |
| Years treated at Clinic, median (IQR) | 9.07 (8.01) | 9.53 (8.05) | 8.72 (7.70) | 0.518 |
| Self-reported ARV use | 0.001 | |||
| Yes | 1049 (95.8) | 554 (97.7) | 495 (93.8) | |
| No | 46 (4.2) | 13 (2.3) | 33 (6.3) | |
| VL, copies/mL | 0.042 | |||
| <200 (undetectable ±±) | 1019 (91.5) | 540 (93.1) | 479 (89.7) | |
| ≥200 | 95 (8.5) | 40 (6.9) | 55 (10.3) | |
| CD4 T cell count, cells/mm3 | 0.009 | |||
| <200 | 65 (5.8) | 22 (3.8) | 43 (8.1) | |
| 200-499 | 295 (26.5) | 160 (27.6) | 135 (25.3) | |
| ≥500 | 754 (67.7) | 398 (68.6) | 356 (66.7) |
UAB Center for AIDS Research Network of Integrated Clinical Systems Patient Reported Outcomes
Computed using T-tests for continuous variables, and Chi-square tests and Fisher’s exact tests (for those with cell counts N≤5) for categorical variables
Including Asian, Native American, Pacific Islander, and multiple races
Centers for Disease Control and Prevention/ Agency for Toxic Substances and Disease Registry/ Geospatial Research, Analysis, and Services Program. CDC/ATSDR Social Vulnerability Index 2018 Database Alabama. https://www.atsdr.cdc.gov/placeandhealth/svi/data_documentation_download.html . Accessed on January 24, 2022.
Centers for Disease Control and Prevention https://www.cdc.gov/hiv/risk/art/index.html
Sociodemographic and clinical variables significantly associated with screening in bivariate analyses included age, race, sexual identity, self-reported ARV use, VL, CD4 count, and number of sexual partners (Table 1). Compared to men who were not, men who were screened were younger, and more likely to be white, identify as homosexual, self-report ARV use, have undetectable VL, and have CD4 counts greater than 500 cells/mm3.
Sexual risk characteristics and screening uptake
Overall, 433 (39.1%) participants reported zero sexual partners, 464 (41.9%) reported one, and 210 (19.0%) reported having multiple sexual partners. Men who were screened were more likely to have multiple partners compared to men not screened (22.8% vs. 14.8%, p=0.002). Among men with one partner, those who were screened were more likely to have a male partner, report unprotected anal and oral sex, and to be concerned about STI exposure or HIV re-exposure (Table 2). In the adjusted regression model, age, gender of partner, and unprotected anal sex were significant factors associated with screening (Table 3). The youngest age group (20-34 years) was almost five times more likely to be screened compared to the middle-aged group (AOR=4.93, 95% CI: 2.34-10.39). Men with a female partner were 96% less likely than men with a male partner to be screened, and men who reported unprotected anal sex were 1.77 times more likely to be screened compared to those who did not.
Table 2.
Sexual risk characteristics and screening uptake within one year of the CNICS PRO* questionnaire among men with one partner (N=464)
| Total Sample N=464 N(%) |
Screened N=235 N(%) |
Not screened N=225 N(%) |
p-value** | |
|---|---|---|---|---|
| Gender of partner | <0.001 | |||
| Male | 326 (70.9) | 226 (96.2) | 100 (44.4) | |
| Female | 134 (29.1) | 9 (3.8) | 125 (55.6) | |
| HIV status of partner | 0.060 | |||
| Positive | 213 (46.3) | 121 (51.7) | 92 (40.7) | |
| Negative | 211 (45.9) | 97 (41.5) | 114 (50.4) | |
| Unknown | 36 (7.8) | 16 (6.8) | 20 (8.9) | |
| Vaginal sex without condom (N=138) *** | ||||
| Yes | 68 (49.3) | 5 (35.7) | 63 (50.8) | 0.284 |
| No | 70 (50.7) | 9 (64.3) | 61 (49.2) | |
| Receptive anal sex without a condom | <0.001 | |||
| Yes | 155 (33.9) | 114 (48.7) | 41 (18.5) | |
| No | 301 (65.9) | 120 (51.3) | 181 (81.5) | |
| Oral sex without a condom or barrier | <0.001 | |||
| Yes | 276 (61.2) | 165 (71.7) | 111 (50.2) | |
| No | 175 (38.8) | 65 (28.3) | 110 (49.8) | |
| Concern of exposure to STI or re-exposure to HIV | 0.005 | |||
| Yes | 32 (7.0) | 24 (10.3) | 8 (3.6) | |
| No | 425 (93.0) | 210 (89.7) | 215 (96.4) |
UAB Center for AIDS Research Network of Integrated Clinical Systems Patient Reported Outcomes
Computed using Chi-square tests and Fisher’s exact tests (for those with cell counts N≤5)
Only 138 responded to this question in the questionnaire
Table 3.
Estimated odds of anal cancer screening* by sociodemographic, clinical, and sexual risk characteristics among men with one partner (N=464)
| Unadjusted OR (95% CI)** | Adjusted OR (95% CI)± | |
|---|---|---|
| Age, years | ||
| 20-34 | 2.65 (1.87-3.74) | 4.93 (2.34-10.39) |
| 35-44 | 1.07 (0.76-1.51) | 1.64 (0.85-3.15) |
| 45-54 | Ref | Ref |
| 55-64 | 0.94 (0.68-1.30) | 1.45 (0.73-2.86) |
| ≥65 | 0.37 (0.20-0.69) | 1.27 (0.35-4.59) |
| Race | ||
| Black | Ref | Ref |
| White | 1.45 (1.14-1.85) | 0.94 (0.55-1.60) |
| Other | 0.80 (0.33-1.93) | 0.64 (0.12-3.47) |
| Sexual identity | ||
| Homosexual | Ref | Ref |
| Heterosexual | 0.05 (0.02-0.09) | 0.83 (0.22-3.12) |
| Bisexual | 1.06 (0.63-1.77) | 1.14 (0.41-3.19) |
| Other | 0.52 (0.28-1.00) | 1.15 (0.19-6.82) |
| Unknown | 0.61 (0.46-0.80) | 1.52 (0.89-2.61) |
| VL, copies/mL | ||
| <200 | Ref | Ref |
| ≥200 | 0.65 (0.42-0.99) | 0.67 (0.23-1.95) |
| Gender of partner | ||
| Male | Ref | Ref |
| Female | 0.03 (0.02-0.07) | 0.04 (0.02-0.10) |
| Receptive anal sex without a condom | ||
| Yes | 4.19 (2.74-6.42) | 1.77 (1.00-3.11) |
| No | Ref | Ref |
| Oral sex without a condom or barrier | ||
| Yes | Ref | Ref |
| No | 0.40 (0.27-0.59) | 1.05 (0.59-1.86) |
| Concern of exposure to STI or re-exposure to HIV | ||
| Yes | 3.07 (1.35-6.99) | 0.95 (0.37-2.44) |
| No | Ref | Ref |
Within one year of completing the UAB Center for AIDS Research Network of Integrated Clinical Systems Patient Reported Outcomes (CNICS PRO) questionnaire
Computed using logistic regression analyses
Adjusted for significant sociodemographic, clinical, and sexual risk characteristics in bivariate analyses, including age, race, sexual identity (including unknown), VL, gender of partner, participation in unprotected anal and oral sex, and concern of exposure to STI or re-exposure HIV
Among 210 men who reported having two or more partners, the majority (85%) had all male partners. Because of limited data and small sample size, a multivariable model would not converge in this population. Among 180 men who reported HIV status of their partners, about 56% (N=101) reported having HIV-positive partners. Among 99 men with HIV-positive partners who reported partner HIV medication use, the majority (N=84; 85%) reported use of all or some of their HIV-positive partners.
Stratifications by age, race, and social vulnerability
When stratified by race, the association between age and screening uptake differed (Table 4). Among black men, the association between age and screening was significant; 43% of those screened were in the youngest group (age 20 to 34 years), 20.9% were 35 to 44 years old, 22.9% were 45 to 54 years old, and less than 15% were 55 years and older. Among white men, the association of screening with age was not statistically significant. Of note, a much smaller proportion of white men screened were in the youngest age group compared to black men (18.6% vs. 43%). The proportion of screened older white men (≥55 years) was double the proportion of black men (33% vs. 15%).
Table 4.
Anal cancer screening* uptake by age stratified by race
| Total Sample | Screened | Not screened | p-value** | |
|---|---|---|---|---|
| Black men, years | 615 | 297 (48.3) | 318 (51.7) | |
| 20-34 | 180 (29.3) | 128 (43.1) | 52 (16.4) | <0.001 |
| 35-44 | 127 (20.7) | 62 (20.9) | 65 (20.4) | |
| 45-54 | 172 (28.0) | 68 (22.9) | 104 (32.7) | |
| 55-64 | 103 (16.8) | 35 (11.8) | 68 (21.4) | |
| ≥65 | 33 (5.4) | 4 (1.4) | 29 (9.1) | |
|
White men, years |
476 | 274 (57.6) | 202 (42.4) | |
| 20-34 | 72 (15.1) | 51 (18.6) | 21 (10.4) | 0.077 |
| 35-44 | 77 (16.2) | 42 (15.3) | 35 (17.3) | |
| 45-54 | 155 (32.6) | 90 (33.0) | 65 (32.2) | |
| 55-64 | 146 (30.7) | 80 (29.2) | 66 (32.7) | |
| ≥65 | 26 (5.5) | 11 (4.0) | 15 (7.4) |
Within one year of completing the UAB Center for AIDS Research Network of Integrated Clinical Systems Patient Reported Outcomes (CNICS PRO) questionnaire
Computed using Chi-square tests and Fisher’s exact tests (for those with cell counts N≤5)
In stratified analyses, SVI and screening were not significantly associated among either black or white men. Because the majority of the participants (N=869; 80%) resided in counties with moderate to high social vulnerability, we examined screening and race more closely in this group. Overall, about 57% of men screened were black and 43% were white (p=0.010; Table 5). Perhaps the most striking difference was among older men (≥65 years) residing in counties with moderate to high social vulnerability (N=52). In this group, only 31% of those screened were black, despite black men representing the majority race (58%), with the majority of men screened being white (69%; p=0.023).
Table 5.
Anal cancer screening* uptake stratified by age and race, among men living in moderate to high social vulnerability counties in Alabama (N=869)
| Screened | Not screened | p-value** | |
|---|---|---|---|
| Total sample | |||
| Black (N=531) | 251 (56.9) | 280 (65.4) | 0.010 |
| White (N=338) | 190 (43.1) | 148 (34.6) | |
| Young men 20-34 years | |||
| Black (N=156) | 113 (76.9) | 43 (71.7) | 0.431 |
| White (N=51) | 34 (23.1) | 17 (28.3) | |
| 35-44 years | |||
| Black (N=111) | 52 (61.9) | 59 (72.8) | 0.135 |
| White (N=54) | 32 (38.1) | 22 (27.2) | |
| 45-54 years | |||
| Black (N=141) | 50 (44.3) | 91 (65.0) | 0.001 |
| White (N=112) | 63 (55.8) | 49 (35.0) | |
| 55-64 years | |||
| Black (N=93) | 32 (38.1) | 61 (56.5) | 0.011 |
| White (N=99) | 52 (61.9) | 47 (43.5) | |
| Older men ≥65 years | |||
| Black (N=30) | 4 (30.8) | 26 (66.7) | 0.023 |
| White (N=22) | 9 (69.2) | 13 (33.3) |
Within one year of completing the UAB Center for AIDS Research Network of Integrated Clinical Systems Patient Reported Outcomes (CNICS PRO) questionnaire
Computed using Chi-square tests and Fisher’s exact tests (for those with cell counts N≤5)
Discussion
The current study found significant missed opportunities for anal cancer screening in a large cohort of PLHIV receiving care in Alabama, with about half of our sample having received annual screening. We identified sociodemographic, clinical, and sexual risk characteristics associated with screening uptake among MLHIV in recent years (2018-2023). Our findings suggest that in particular, older, black men living in moderate to high SVI counties may be at most risk of missing out on the benefits of screening.
Age was a significant factor when examining screening uptake. Among men with one partner, the youngest age group was almost five times more likely to be screened compared to middle aged men. It is promising that in our sample, younger MLHIV were being screened, as some experts now recommend screening initiation at 35 years of age among PLHIV independent of HPV-vaccination status (Hirsch et al., 2022). However, these findings also suggest that middle-aged and older men may be missing out on early detection of anal dysplasia and treatment, which could substantially reduce their risk of developing cancer as they age. As national guidelines are expected soon following the ANCHOR trial, we are optimistic that older PLHIV in the South will receive more consistent annual screening (Palefsky et al., 2022).
Findings from our stratified analyses suggest a significant racial disparity, particularly among older men, with older black MLHIV being the least likely to be screened. Perhaps the most striking differences in race and screening was among men ≥65 years of age living in counties with moderate to high social vulnerability, with only a third of men screened being black. Even after adjusting for county-level social vulnerability, black men were less likely to be screened compared to white men. This is worrisome as black men are more at-risk of developing anal cancer, and among black Americans, high SVI has been associated with increased risk of HIV infection (Dailey et al., 2022). It is critical that screening efforts focus on older, black men in the South to reduce the burden of anal cancer in this population. Furthermore, black Americans and other racial and ethnic minorities living in regions with high social vulnerability have been found to have lower linkage to care and lower rates of viral suppression (Dailey et al., 2022; Elenwa et al., 2023).
In our study, men who reported engaging in unprotected anal sex and men with multiple sexual partners, the majority identifying as MSM, are being screened. However, in our study, men who reported having a female partner were much less likely to be screened. It is possible that some in this group have a history of engaging in sex with both men and women but do not identify as homosexual, known as being on the “down low,” and may be missing out on the benefits of anal cancer screening (Bond et al., 2009; Malebranche, 2008; Millett et al., 2005). Furthermore, MLHIV without a history of receptive anal sex can acquire high-risk HPV types through other sexual practices or self-inoculation, could still be at risk of anal precancer and cancer, and should not miss out on the benefits of screening (Ong et al., 2016; Pamnani et al., 2016; Petca et al., 2020; Wei et al., 2023).
The current study’s findings should be interpreted with several limitations in mind. First, we had some missing data which limited our analyses. For example, about 40% of self-reported sexual identity was missing. Additionally, among men with multiple sexual partners, about 50% of the data regarding HIV-negative partner PrEP use and HIV-positive partner medication use was missing. Since having multiple sexual partners is associated with other risky sexual behaviors such as unprotected sex and nondisclosure of HIV status and is a significant risk factor of STIs, further research should examine barriers to screening in this population (Jansen et al., 2020; Kalichman et al., 2007). Second, sexual risk characteristic correlates of screening could not be examined among men who did not report having current sexual partner(s). Because of the nature of the questionnaire items collected as sexual risk measures (gender of partner(s), HIV status of partner(s), HIV medication/ PreP use among partner(s), and participation in vaginal, anal, and oral sex), these are not collected among men who report no current sexual partners. Although we cannot examine sexual risk characteristics associated with screening in the current study among men who do not report current sexual partners, further research should include them, as they may still be at risk from prior HPV acquisition.
Third, our SVI analyses were based on the county within which the patient lived; individual-level socioeconomic status was not examined in the current study. Additionally, our analyses were limited geographically, as our sample only includes men residing in Alabama and the majority live in moderate to high SVI counties. Furthermore, our analyses only included men at one HIV clinic which may limit the generalizability of the findings. Further exploration of barriers to screening among a larger sample in the South is needed.
Lastly, although much of the current screening literature focuses on MSM as they represent the highest risk group in the development of anal cancer proportionally, females represent a larger number of anal cancer cases overall and should not be overlooked in screening efforts (SEER, 2023). In fact, in the U.S., the number of cases of anal cancer among women are about two-fold the cases among men (ACS, 2023). Additionally, recent reports suggest that women living with HIV (WLHIV) have low perceived risk of anal cancer, and limited knowledge of screening methods (Rodriguez et al., 2021; J. Wells et al., 2022). Barriers of screening among WLHIV was beyond the scope of the current study but should be examined in future research. Despite these limitations, the current study identified potential barriers to anal cancer screening, including older age, black race, and having a female partner, in a large group of MLHIV in Alabama. Importantly, our findings suggest a significant racial disparity in moderate to high SVI counties, with older black MLHIV being the least likely to be screened. Further research utilizing qualitative and mixed methods approaches is needed to understand why these barriers exist and to aid in promoting screening in the South.
In conclusion, MLHIV who are older, heterosexual, black, or living in counties in Alabama with moderate to high social vulnerability may be less likely to access secondary preventative care of anal cancer and receive annual screening compared to their counterparts. Future research is needed to understand how to address these barriers and promote screening in MLHIV in the South. As anal cancer screening guidelines are expected to be updated in the U.S. very soon following the results from the ANCHOR study (Palefsky et al., 2022), it will be critical to monitor screening uptake among PLHIV in the South to ensure that there are not missed opportunities to preventative anal cancer care in this understudied population.
Acknowledgments
We would like to thank the study participants and the UAB Research and Informatics Service Center (RISC) for providing the data from the 1917 Clinic.
Funding
This research was supported by the UAB Center For AIDS Research (CFAR), an NIH funded program (P30 AI027767) that was made possible by the following institutes: NIAID, NCI, NICHD, NHLBI, NIDA, NIMH, NIA, NIDDK, NIGMS, NIMHD, FIC, NIDCR, and OAR. Additionally, this research is supported by the NCI under Grant [number 1F31CA261013-01A1].
Footnotes
Declaration of Interest Statement
The authors report there are no competing interests to declare.
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