Abstract
Purpose
People with HIV (PWH) in the United States (U.S.) are disproportionately impacted by human papillomavirus-related cancers. We aimed to identify sociodemographic, health, and social predictors of anal and cervical cancer screening uptake among adults with and without HIV.
Methods
We implemented a cross-sectional survey between April and June 2024 among adult patients receiving care at a community-based clinic network (predominantly based in Florida, U.S.) that delivers HIV prevention and treatment services. Outcomes included any receipt of anal cancer screening and guideline-adherent receipt of cervical cancer screening among eligible participants. We computed adjusted prevalence ratios (aPRs) to identify multilevel predictors associated with screening uptake.
Results
Among the survey respondents, 412 (42%) were eligible for anal cancer screening and 294 (30%) for cervical cancer screening. Participants eligible for anal cancer screening included 88.8% living with HIV and 82.3% men. Men with HIV were more likely to receive anal cancer screening compared to men without HIV (aPR 1.57, 95% CI 1.08, 2.27). Among men with HIV, anal cancer screening uptake was associated with any precancer diagnosis and having three or more comorbidities. Women eligible for cervical cancer screening included 43.5% living with HIV. Women with HIV were less likely to receive guideline-adherent cervical cancer screening compared to women without HIV (aPR 0.60, 95% CI 0.47, 0.77). HIV-related disclosure concerns were associated with lower guideline-adherent cervical screening uptake among women with HIV (aPR 0.75, 95% CI 0.60, 0.94).
Conclusion
Screening-eligible participants with HIV were more likely to receive anal cancer screening and less likely to receive cervical cancer screening. Anal and cervical cancer screening uptake differed among subpopulations of people with HIV, including by race/ethnicity, household size, any precancer, comorbidities, and HIV-related stigma. Efforts to improve anal and cervical cancer screening uptake among high-risk and screening-eligible populations are needed.
Keywords: Anal cancer, Cervical cancer, Cancer screening, People with HIV, Human papillomavirus
Introduction
In the United States (U.S.), people with HIV (PWH) are disproportionately impacted by human papillomavirus (HPV)-related cancers, including anal and cervical cancers [1–3]. High-risk HPV causes more than 90% of anal and cervical cancer cases [4, 5]. Compared to people without HIV (PWoH), PWH are 17 times more likely to develop anal cancer, and women with HIV are 4 times more likely to develop cervical cancer [6]. This disproportionate burden among PWH is attributable to many factors, including HIV-related immunosuppression and the high prevalence of HPV–HIV co-infection, as HPV is more likely to persist and progress to cancer among PWH [7, 8]. Other health system factors, such as barriers to screening, delays in diagnosis, and limited access to appropriate treatment also contribute to the higher rates of advanced-stage diagnoses and increased mortality among PWH [9–11].
Both anal and cervical cancers are characterized by well-defined and detectable premalignant lesions, making them particularly suitable for early detection through cancer screening [12, 13]. The removal of high-grade squamous intraepithelial lesions (HSILs) can prevent the progression of precancerous lesions to anal or cervical cancer or allow for the early treatment of cancer [13, 14]. Guidelines for cervical cancer screening exist, including the U.S. Preventive Services Task Force (USPSTF) guideline [14] for women without HIV (WWoH) and the Infectious Diseases Society of America (IDSA) guidance [15] for women with HIV (WWH). While formal anal cancer screening guidelines are more recent, the landmark Anal Cancer/HSIL Outcomes Research (ANCHOR) study demonstrated a significant reduction in anal cancer incidence among PWH when treating HSILs compared to active monitoring [13, 16]. The seminal findings of the ANCHOR study served as the basis for the International Anal Neoplasia Society (IANS) consensus guidelines for anal cancer screening [16].
Although guideline-concordant screening for high-risk populations has demonstrated reductions in both anal and cervical cancer mortality [14, 16], gaps in screening uptake exist for marginalized populations in the US, such as those living with HIV. Few published studies have been conducted to understand predictors of screening among PWH receiving care in an HIV community clinic setting. To address this gap, this study aimed to identify sociodemographic, health, and social predictors of any anal cancer screening uptake and guideline-adherent cervical cancer screening uptake by HIV status among adults receiving HIV prevention and treatment services within a network of Ryan White community clinics. Insights into the unique barriers faced by PWH, a patient population that is at especially high risk of HPV-related cancers, are critical to increasing anal and cervical cancer screening behaviors.
Methods
Study design and participants
This study was supported through a novel initiative of Moffitt Cancer Center’s Office of Community Outreach and Engagement (Moffitt COE) in collaboration with CAN Community Health (CAN). CAN is a community-based Ryan White-funded health clinic network (predominantly based in Florida, U.S.) that delivers both HIV prevention and treatment services to a large patient population of PWH and PWoH at high risk for HIV. CAN also provides primary care, testing and prevention services for non-HIV sexually transmitted illnesses, dental care, specialist referral, mental health counseling, and social services support. In the fiscal year 2024–2025, CAN served more than 31,100 unique patients and their patient demographics included 35% White, 35% Black, 18% Hispanic/Latino, 69% male, and 41% homosexual [17]. To better understand the cancer-related needs of the CAN patient population, Moffitt’s COE team collaborated with CAN leadership to develop and implement a survey.
The survey was conducted between April and June 2024 using REDCap, a web-based electronic data capture platform [18, 19] and was distributed through an anonymous link via Phreesia, CAN’s electronic patient intake system. The survey included questions on participant sociodemographic and health characteristics, cancer prevention behaviors, perceived health system experiences, and social exposures. The survey took approximately 25 min to complete and was available in English and Spanish. Participants were compensated with a $25 gift card following participation.
The inclusion criteria for survey participation were determined in Phreesia and included (1) adults aged 18 years or older; (2) received care at least once at CAN between 2022 and 2023; (3) able to read and write in English or Spanish; and (4) active users of Phreesia. The focus of this current study was on the uptake of anal and cervical cancer screening. Therefore, we restricted analyses to participants who qualified for anal and/or cervical cancer screenings based on clinical guidelines, determined by participants’ self-reported survey responses. Participants recommended for anal cancer screening under the IANS guideline included (1) MSM and transgender women with HIV aged ≥35 years and (2) other people with HIV, and MSM and transgender women without HIV aged ≥45 years [16]. For WWoH, the USPSTF guideline recommends cervical cancer screening every three years for women aged 21 to 65 years [14]. For WWH, the IDSA guidance recommends cervical cancer screening annually for women aged 21 and older [15]. This study was reviewed and deemed exempt by Moffitt’s Institutional Review Board of Record, Advarra (Pro00077872). Informed consent was obtained from all participants. This study was reported in accordance with the Strengthening the Reporting of Observational Studies in Epidemiology guidelines [20].
Anal and cervical cancer screening uptake
Any anal cancer screening uptake was assessed by asking the questions: “Have you ever had an anal Pap test?” and “Has a doctor or medical practitioner ever inserted a tube-shaped device or scope in your anus or rectum to look for hemorrhoids, fissures, infections, or some cancers? This is also known as high resolution anoscopy.” Response options included “Yes,” “No,” and “Don’t know.” Any anal cancer screening receipt was classified as ever having an anal Pap test or anoscopy. Cervical cancer screening uptake was assessed by asking: “How long ago did you have your most recent Pap test to check for cervical cancer?” Response options included “A year ago or less,” “More than 1, up to 2 years ago,” “More than 2, up to 3 years ago,” “More than 3, up to 5 years ago,” “More than 5 years ago,” “I have never had a Pap test,” and “Not applicable.” Consistent with cervical cancer screening guidelines [14, 15], responses were dichotomized into guideline adherent (3 years ago or less for WWoH, and one year ago or less for WWH) and non-guideline adherent.
Independent variables
Participant characteristics
Self-reported sociodemographic and health characteristics derived from the survey included age, race/ethnicity, sex, sexual orientation, marital status, highest educational attainment, household size, health insurance type, HIV status, years since HIV diagnosis, any precancer diagnosis, history of cancer, family history of cancer, history of smoking, illegal substance use, Body Mass Index, and comorbidities (diabetes, high blood sugar, high blood pressure, heart condition, chronic lung disease, arthritis or rheumatism, and depression or anxiety disorder).
Health system experiences
Perceived health system experiences were collected, including provider dependability, patient–provider communication, and healthcare system distrust. Provider dependability was assessed by the question: “How much can you depend on your doctors and other health professionals to give you the care you need?” Responses were dichotomized for analysis (a lot or a great deal vs. not at all, not very much, or somewhat).
Quality of patient–provider communication was assessed using an adapted “How Well Doctors Communicate” scale used by the Consumer Assessment of Healthcare Providers and Systems Health Plan Survey [21]. The scale included four questions: “In the last 12 months, how often did your personal doctor…” (1) “Explain things in a way that was easy to understand?” (2) “Listen carefully to you?” (3) “Show respect for what you had to say?” and (4) “spend enough time with you?” Responses were scored from 1 (never) to 5 (always), with higher scores indicating higher-quality communication.
Healthcare system distrust was assessed using the Revised Health Care System Distrust Scale [22]. The scale included nine items: (1) “The health care system does its best to make patients’ health better,” (2) “The health care system covers up its mistakes,” (3) “Patients receive high quality medical care from the health care system,” (4) “The health care system makes too many mistakes,” (5) “The health care system puts making money above patients’ needs,” (6) “The health care system gives excellent medical care,” (7) “Patients get the same medical treatment from the health care system no matter what the patients’ race or ethnicity,” (8) “The health care system lies to make money,” and (9) “The health care system experiments on patients without them knowing.” Items one, three, six, and seven were reverse coded, and responses were scored from 1 (strongly disagree) to 5 (strongly agree), with higher scores indicating greater distrust in the healthcare system.
HIV stigma
HIV-related stigma and discrimination was assessed by the HIV Stigma Scale short form [23]. The 12-item scale assessed four subscale domains of HIV-related stigma, including (1) personalized stigma (e.g., rejection and avoidance by close social contacts), (2) disclosure concerns (e.g., having to keep one’s HIV status a secret), (3) concerns about public attitudes (e.g., consequences of living with HIV from people in general), and (4) negative self-image (e.g., shame and guilt over one’s HIV status) [23]. Responses were scored from 1 (strongly disagree) to 4 (strongly agree) with higher scores indicating greater HIV stigma.
Statistical analyses
We examined the health system experience and HIV stigma scale scores for missingness. Consistent with prior literature [24], mean imputations were performed for scale scores with item-missingness of 20% or less. Mean imputation with modest amounts of missing data was found to be a reliable approach that yields minimal bias [24]. Participants with more than 20% of items missing on the scale were excluded from the analysis of that scale (7% of participants for the overall HIV stigma scale and the disclosure concerns subscale; 6% of participants for the concerns about public attitudes subscale; 5% of participants for the negative self-image subscale; 4% of participants for the personalized stigma subscale; 3% of participants for the patient–provider communication scale; and 1% of participants for the healthcare system distrust scale).
We described participant characteristics and cancer screening uptake for the overall sample and compared each variable by HIV status using ordinary linear regression for continuous variables and Pearson’s χ2 test for categorical variables. To estimate the association between each predictor with cancer screening uptake, we computed adjusted prevalence ratios (aPRs) and 95% confidence intervals (CIs) using multivariable Poisson regression with a log-link function and robust standard errors. The Andersen Behavioral Model and prior literature that assessed associations of cancer prevention behaviors guided the selection of predictors, which include sociodemographics, health history and needs, and healthcare perceptions, engagement, and barriers [25, 26]. All models were adjusted for age (years) and race/ethnicity [non-Hispanic (NH)-White, NH-Black, Hispanic/Latino, NH-other race, and unknown]. Based on disparate cancer risk and screening outcomes among populations reported in previous literature, models for anal cancer screening were stratified by HIV status and sex at birth (men without HIV, MWoH, men with HIV, MWH, WWoH, and WWH) [27], and models for cervical cancer screening were stratified by HIV status (WWoH and WWH) [5]. A complete case approach of the outcomes was used. Missing categorical independent variables were included in the analysis as a separate category but were not shown for brevity [28]. All analyses were performed in Stata v.17 (StataCorp, College Station, TX, USA).
Results
Participant characteristics
Characteristics of participants who were eligible for anal cancer screening are shown in Table 1. Among the 412 anal cancer screening-eligible participants, the median age was 56.0 years, 88.8% were living with HIV, and 82.3% were male. The racial and ethnic composition included 57.3% NH-White, 19.2% NH-Black, 16.5% Hispanic/Latino, and 6.6% NH-other race. Two-thirds (66.0%) of participants identified as lesbian or gay. Marital status included never married (43.2%), now married (31.3%), and separated, divorced, or widowed (24.5%).
Table 1.
Characteristics of participants eligible for anal cancer screening overall and by HIV status
| Characteristics | No. (%) or median (IQR) | pa | ||
|---|---|---|---|---|
| Overall (n=412) | Participants without HIV (n=46) | Participants with HIV (n=366) | ||
| Sociodemographic | ||||
| Age (years) | ||||
| 35–44 | 71 (17.2%) | 0 (0.0%) | 71 (19.4%) | 0.006 |
| 45–54 | 123 (29.9%) | 20 (43.5%) | 103 (28.1%) | |
| 55–64 | 136 (33.0%) | 17 (37.0%) | 119 (32.5%) | |
| ≥65 | 82 (19.9%) | 9 (19.6%) | 73 (19.9%) | |
| Median (IQR) | 56.0 (47.0–63.0) | 57.0 (50.0–64.0) | 55.5 (46.0–63.0) | 0.075 |
| Race/ethnicity | ||||
| White, non-Hispanic | 236 (57.3%) | 34 (73.9%) | 202 (55.2%) | 0.166 |
| Black, non-Hispanic | 79 (19.2%) | 4 (8.7%) | 75 (20.5%) | |
| Hispanic/Latino | 68 (16.5%) | 6 (13.0%) | 62 (16.9%) | |
| Other, non-Hispanic | 27 (6.6%) | 2 (4.3%) | 25 (6.8%) | |
| Unknown | 2 (0.5%) | 0 (0.0%) | 2 (0.5%) | |
| Sex at birth | ||||
| Male | 339 (82.3%) | 46 (100.0%) | 293 (80.1%) | <0.001 |
| Female | 73 (17.7%) | 0 (0.0%) | 73 (19.9%) | |
| Sexual orientation | ||||
| Straight | 90 (21.8%) | 0 (0.0%) | 90 (24.6%) | 0.003 |
| Lesbian or gay | 272 (66.0%) | 38 (82.6%) | 234 (63.9%) | |
| Bisexual | 39 (9.5%) | 7 (15.2%) | 32 (8.7%) | |
| Other | 3 (0.7%) | 0 (0.0%) | 3 (0.8%) | |
| Unknown | 8 (1.9%) | 1 (2.2%) | 7 (1.9%) | |
| Marital status | ||||
| Never married | 178 (43.2%) | 18 (39.1%) | 160 (43.7%) | 0.795 |
| Now married | 129 (31.3%) | 15 (32.6%) | 114 (31.1%) | |
| Separated/divorced/widowed | 101 (24.5%) | 13 (28.3%) | 88 (24.0%) | |
| Unknown | 4 (1.0%) | 0 (0.0%) | 4 (1.1%) | |
| Highest educational attainment | ||||
| High school (and equivalent) or less | 97 (23.5%) | 4 (8.7%) | 93 (25.4%) | <0.001 |
| Some college (including vocational training or associate’s degree) | 160 (38.8%) | 13 (28.3%) | 147 (40.2%) | |
| Bachelor’s degree or more | 144 (35.0%) | 29 (63.0%) | 115 (31.4%) | |
| Other | 3 (0.7%) | 0 (0.0%) | 3 (0.8%) | |
| Unknown | 8 (1.9%) | 0 (0.0%) | 8 (2.2%) | |
| Household size | ||||
| 1 | 162 (39.3%) | 21 (45.7%) | 141 (38.5%) | 0.302 |
| 2 | 144 (35.0%) | 16 (34.8%) | 128 (35.0%) | |
| 3+ | 74 (18.0%) | 4 (8.7%) | 70 (19.1%) | |
| Unknown | 32 (7.8%) | 5 (10.9%) | 27 (7.4%) | |
| Insurance type (multiple may apply) | ||||
| Employer or union | 127 (30.8%) | 24 (52.2%) | 103 (28.1%) | <0.001 |
| Direct purchase | 55 (13.3%) | 9 (19.6%) | 46 (12.6%) | 0.171 |
| Medicare | 119 (28.9%) | 10 (21.7%) | 109 (29.8%) | 0.283 |
| Medicaid | 92 (22.3%) | 2 (4.3%) | 90 (24.6%) | 0.005 |
| Other | 48 (11.7%) | 2 (4.3%) | 46 (12.6%) | 0.138 |
| Uninsured | 4 (1.0%) | 1 (2.2%) | 3 (0.8%) | 0.307 |
| Health characteristics | ||||
| Long-term (≥ 10 years) survivor of HIV | ||||
| No | – | – | 69 (18.9%) | – |
| Yes | – | – | 276 (75.4%) | |
| Unknown | – | – | 21 (5.7%) | |
| Ever diagnosed with precancer | ||||
| No | 351 (85.4%) | 40 (87.0%) | 311 (85.2%) | 0.751 |
| Yes | 60 (14.6%) | 6 (13.0%) | 54 (14.8%) | |
| Ever diagnosed with cancer | ||||
| No | 342 (83.0%) | 41 (89.1%) | 301 (82.2%) | 0.241 |
| Yes | 70 (17.0%) | 5 (10.9%) | 65 (17.8%) | |
| Family history of cancer | ||||
| No | 104 (25.2%) | 16 (34.8%) | 88 (24.0%) | 0.267 |
| Yes | 259 (62.9%) | 26 (56.5%) | 233 (63.7%) | |
| Unknown | 49 (11.9%) | 4 (8.7%) | 45 (12.3%) | |
| Smoked at least 100 cigarettes | ||||
| No | 183 (44.4%) | 23 (50.0%) | 160 (43.7%) | 0.419 |
| Yes | 229 (55.6%) | 23 (50.0%) | 206 (56.3%) | |
| Used illegal substances in the past year | ||||
| No | 214 (51.9%) | 22 (47.8%) | 192 (52.5%) | 0.574 |
| Yes | 193 (46.8%) | 24 (52.2%) | 169 (46.2%) | |
| Unknown | 5 (1.2%) | 0 (0.0%) | 5 (1.4%) | |
| Body Mass Index | ||||
| Underweight | 4 (1.0%) | 0 (0.0%) | 4 (1.1%) | 0.283 |
| Healthy weight | 111 (27.5%) | 11 (23.9%) | 100 (27.9%) | |
| Overweight | 152 (37.6%) | 23 (50.0%) | 129 (36.0%) | |
| Obesity | 137 (33.9%) | 12 (26.1%) | 125 (34.9%) | |
| Number of comorbidities (out of 7)b | ||||
| 0 | 77 (18.7%) | 7 (15.2%) | 70 (19.1%) | 0.533 |
| 1 | 108 (26.2%) | 17 (37.0%) | 91 (24.9%) | |
| 2 | 77 (18.7%) | 7 (15.2%) | 70 (19.1%) | |
| 3+ | 110 (26.7%) | 11 (23.9%) | 99 (27.0%) | |
| Unknown | 40 (9.7%) | 4 (8.7%) | 36 (9.8%) | |
| Health system experiences | ||||
| How much can you depend on your doctors and other health professionals to give you the care you need? | ||||
| Not at all/not very much/somewhat | 58 (14.1%) | 2 (4.3%) | 56 (15.3%) | 0.044 |
| A lot/a great deal | 354 (85.9%) | 44 (95.7%) | 310 (84.7%) | |
| Patient-provider communication (range 1–5), median score (IQR)c | 5.0 (4.2–5.0) | 5.0 (4.5–5.0) | 5.0 (4.2–5.0) | 0.268 |
| Healthcare system distrust (range 1–5), median score (IQR)c | 2.0 (1.4–2.7) | 1.8 (1.3–2.6) | 2.0 (1.4–2.7) | 0.307 |
| HIV stigma | ||||
| Overall HIV stigma (range 1–4), median score (IQR)c | – | – | 2.3 (1.8–2.8) | – |
| Personalized stigma (range 1–4), median score (IQR)c | – | – | 2.0 (1.0–2.3) | – |
| Disclosure concerns (range 1–4), median score (IQR)c | – | – | 3.0 (2.3–3.7) | – |
| Concerns with public attitudes (range 1–4), median score (IQR)c | – | – | 2.7 (2.0–3.0) | – |
| Negative self-image (range 1–4), median score (IQR)c | – | – | 2.0 (1.0–2.7) | – |
ap Values were computed using ordinary linear regression for continuous variables and Pearson’s χ2 test for categorical variables
bComorbidities included: high blood sugar; diabetes; high blood pressure or hypertension; heat conditions, heart attack, angina, or congestive heart failure; chronic lung disease, asthma, emphysema, or chronic bronchitis; arthritis or rheumatism; and depression or anxiety disorder
cParticipants with >20% of items missing on the scale were excluded
Characteristics of participants who were eligible for cervical cancer screening are shown in Table 2. Among the 294 cervical cancer screening-eligible women, the median age was 38.0 years, and 43.5% were living with HIV. The racial and ethnic composition included 30.3% NH-White, 37.4% NH-Black, 22.4% Hispanic/Latino, and 8.5% NH-other race. Most (71.4%) women identified as straight, and 50.0% were never married.
Table 2.
Characteristics of women eligible for cervical cancer screening overall and by HIV status
| Characteristics | No. (%) or median (IQR) | pa | ||
|---|---|---|---|---|
| Overall (n=294) | Participants without HIV (n=166) | Participants with HIV (n=128) | ||
| Sociodemographic | ||||
| Age (years) | ||||
| 21–29 | 84 (28.6%) | 77 (46.4%) | 7 (5.5%) | <0.001 |
| 30–39 | 84 (28.6%) | 53 (31.9%) | 31 (24.2%) | |
| 40–49 | 58 (19.7%) | 26 (15.7%) | 32 (25.0%) | |
| 50–65 | 56 (19.0%) | 10 (6.0%) | 46 (35.9%) | |
| >65 | 12 (4.1%) | – | 12 (9.4%) | |
| Median (IQR) | 38.0 (29.0–48.0) | 30.0 (25.0–38.0) | 47.0 (38.0–58.0) | <0.001 |
| Race/ethnicity | ||||
| White, non-Hispanic | 89 (30.3%) | 48 (28.9%) | 41 (32.0%) | 0.177 |
| Black, non-Hispanic | 110 (37.4%) | 55 (33.1%) | 55 (43.0%) | |
| Hispanic/Latino | 66 (22.4%) | 44 (26.5%) | 22 (17.2%) | |
| Other, non-Hispanic | 25 (8.5%) | 17 (10.2%) | 8 (6.2%) | |
| Unknown | 4 (1.4%) | 2 (1.2%) | 2 (1.6%) | |
| Sexual orientation | ||||
| Straight | 210 (71.4%) | 106 (63.9%) | 104 (81.2%) | 0.020 |
| Lesbian or gay | 11 (3.7%) | 9 (5.4%) | 2 (1.6%) | |
| Bisexual | 46 (15.6%) | 32 (19.3%) | 14 (10.9%) | |
| Other | 13 (4.4%) | 10 (6.0%) | 3 (2.3%) | |
| Unknown | 14 (4.8%) | 9 (5.4%) | 5 (3.9%) | |
| Marital status | ||||
| Never married | 147 (50.0%) | 96 (57.8%) | 51 (39.8%) | <0.001 |
| Now married | 64 (21.8%) | 38 (22.9%) | 26 (20.3%) | |
| Separated/divorced/widowed | 79 (26.9%) | 29 (17.5%) | 50 (39.1%) | |
| Unknown | 4 (1.4%) | 3 (1.8%) | 1 (0.8%) | |
| Highest educational attainment | ||||
| High school (and equivalent) or less | 109 (37.1%) | 57 (34.3%) | 52 (40.6%) | 0.415 |
| Some college (including vocational training or associate’s degree) | 119 (40.5%) | 66 (39.8%) | 53 (41.4%) | |
| Bachelor’s degree or more | 52 (17.7%) | 34 (20.5%) | 18 (14.1%) | |
| Unknown | 14 (4.8%) | 9 (5.4%) | 5 (3.9%) | |
| Household size | ||||
| 1 | 75 (25.5%) | 39 (23.5%) | 36 (28.1%) | 0.398 |
| 2 | 69 (23.5%) | 45 (27.1%) | 24 (18.8%) | |
| 3+ | 126 (42.9%) | 69 (41.6%) | 57 (44.5%) | |
| Unknown | 24 (8.2%) | 13 (7.8%) | 11 (8.6%) | |
| Insurance type (multiple may apply) | ||||
| Employer or union | 68 (23.1%) | 53 (31.9%) | 15 (11.7%) | <0.001 |
| Direct purchase | 28 (9.5%) | 18 (10.8%) | 10 (7.8%) | 0.673 |
| Medicare | 34 (11.6%) | 3 (1.8%) | 31 (24.2%) | <0.001 |
| Medicaid | 116 (39.5%) | 53 (31.9%) | 63 (49.2%) | 0.009 |
| Other | 35 (11.9%) | 19 (11.4%) | 16 (12.5%) | 0.962 |
| Uninsured | 15 (5.1%) | 15 (9.0%) | 0 (0.0%) | 0.002 |
| Health characteristics | ||||
| Long-term (≥ 10 years) survivor of HIV | ||||
| No | – | – | 27 (21.1%) | – |
| Yes | – | – | 88 (68.8%) | |
| Unknown | – | – | 13 (10.2%) | |
| Ever diagnosed with precancer | ||||
| No | 267 (91.1%) | 158 (95.8%) | 109 (85.2%) | 0.002 |
| Yes | 26 (8.9%) | 7 (4.2%) | 19 (14.8%) | |
| Ever diagnosed with cancer | ||||
| No | 275 (93.9%) | 164 (98.8%) | 111 (87.4%) | <0.001 |
| Yes | 18 (6.1%) | 2 (1.2%) | 16 (12.6%) | |
| Family history of cancer | ||||
| No | 74 (25.2%) | 47 (28.3%) | 27 (21.1%) | 0.363 |
| Yes | 182 (61.9%) | 98 (59.0%) | 84 (65.6%) | |
| Unknown | 38 (12.9%) | 21 (12.7%) | 17 (13.3%) | |
| Smoked at least 100 cigarettes | ||||
| No | 186 (63.3%) | 123 (74.1%) | 63 (49.2%) | <0.001 |
| Yes | 108 (36.7%) | 43 (25.9%) | 65 (50.8%) | |
| Used illegal substances in the past year | ||||
| No | 156 (53.1%) | 77 (46.4%) | 79 (61.7%) | 0.031 |
| Yes | 128 (43.5%) | 82 (49.4%) | 46 (35.9%) | |
| Unknown | 10 (3.4%) | 7 (4.2%) | 3 (2.3%) | |
| Body mass index | ||||
| Underweight | 4 (1.4%) | 3 (1.9%) | 1 (0.9%) | 0.019 |
| Healthy weight | 85 (30.6%) | 56 (34.8%) | 29 (24.8%) | |
| Overweight | 58 (20.9%) | 39 (24.2%) | 19 (16.2%) | |
| Obesity | 131 (47.1%) | 63 (39.1%) | 68 (58.1%) | |
| Number of comorbidities (out of 7)b | ||||
| 0 | 99 (33.7%) | 77 (46.4%) | 22 (17.2%) | <0.001 |
| 1 | 69 (23.5%) | 41 (24.7%) | 28 (21.9%) | |
| 2 | 58 (19.7%) | 25 (15.1%) | 33 (25.8%) | |
| 3+ | 42 (14.3%) | 10 (6.0%) | 32 (25.0%) | |
| Unknown | 26 (8.8%) | 13 (7.8%) | 13 (10.2%) | |
| Health system experiences | ||||
| How much can you depend on your doctors and other health professionals to give you the care you need? | ||||
| Not at all/not very much/somewhat | 74 (25.2%) | 51 (30.7%) | 23 (18.0%) | 0.012 |
| A lot/a great deal | 220 (74.8%) | 115 (69.3%) | 105 (82.0%) | |
| Patient-provider communication (range 1–5), median score (IQR)c | 5.0 (4.0–5.0) | 4.5 (3.5–5.0) | 5.0 (4.0–5.0) | 0.004 |
| Healthcare system distrust (range 1–5), median score (IQR)c | 2.3 (1.6–3.0) | 2.6 (1.7–3.0) | 2.1 (1.4–2.8) | 0.048 |
| HIV stigma | ||||
| Overall HIV stigma (range 1–4), median score (IQR)c | – | – | 2.5 (2.0–3.1) | – |
| Personalized stigma (range 1–4), median score (IQR)c | – | – | 2.0 (1.3–3.0) | – |
| Disclosure concerns (range 1–4), median score (IQR)c | – | – | 3.0 (2.3–3.7) | – |
| Concerns with public attitudes (range 1–4), median score (IQR)c | – | – | 3.0 (2.3–4.0) | – |
| Negative self-image (range 1–4), median score (IQR)c | – | – | 2.0 (1.0–3.0) | – |
ap Values were computed using ordinary linear regression for continuous variables and Pearson’s χ2 test for categorical variables
bComorbidities included: high blood sugar; diabetes; high blood pressure or hypertension; heat conditions, heart attack, angina, or congestive heart failure; chronic lung disease, asthma, emphysema, or chronic bronchitis; arthritis or rheumatism; and depression or anxiety disorder
cParticipants with >20% of items missing on the scale were excluded
Predictors of anal and cervical cancer screening uptake
Among the participants eligible for anal cancer screening, 58.6% reported having been screened for anal cancer (61.0% of PWH and 42.5% of PWoH; p=0.027). Among men, 63.2% had received anal cancer screening (67.3% of MWH and 42.5% of MWoH; p=0.003). Among WWH, 41.5% had received anal cancer screening. After adjustments for participant characteristics, MWH were more likely to receive anal cancer screening compared to MWoH (aPR 1.57, 95% CI 1.08, 2.27, Table 3). Among MWH, factors associated with higher anal cancer screening uptake included NH-other race compared to NH-White (aPR 1.40, 95% CI 1.15, 1.71), being diagnosed with any precancer (aPR 1.37, 95% CI 1.15, 1.64) and having three or more comorbidities (aPR 1.51, 95% CI 1.07, 2.14). Living in a household with three or more people was associated with lower anal cancer screening uptake among MWH (aPR 0.62, 95% CI 0.40, 0.98). Among WWH, living in a household with two people was associated with higher anal cancer screening uptake (aPR 2.87, 95% CI 1.26, 6.51).
Table 3.
Adjusted associations of sociodemographic, health, and social predictors with any anal cancer screening uptake among screening-eligible participants
| Characteristics | aPR (95% CI)a | |
|---|---|---|
| Men | Women | |
| Living with HIV | ||
| No | Ref. | – |
| Yes | 1.57* (1.08, 2.27) | – |
| Men without HIV | Men with HIV | Women with HIV | |
|---|---|---|---|
| Sociodemographic | |||
| Age (years) | 0.96 (0.92, 1.00) | 1.00 (0.99, 1.02) | 1.01 (0.98, 1.05) |
| Race/ethnicity | |||
| White, non-Hispanic | Ref. | Ref. | Ref. |
| Black, non-Hispanic | 1.46 (0.70, 3.04) | 0.82 (0.55, 1.21) | 0.95 (0.52, 1.73) |
| Hispanic/Latino | 0.79 (0.24, 2.63) | 1.03 (0.75, 1.41) | 0.36 (0.10, 1.33) |
| Other, non-Hispanic | NC | 1.40*** (1.15, 1.71) | 0.50 (0.09, 2.91) |
| Sexual orientation | |||
| Straight | – | Ref. | Ref. |
| Lesbian or gay | Ref. | 1.49 (0.95, 2.32) | NC |
| Bisexual | 0.82 (0.21, 3.30) | 1.50 (0.88, 2.57) | 0.97 (0.33, 2.89) |
| Other | NC | NC | NC |
| Marital status | |||
| Never married | Ref. | Ref. | Ref. |
| Now married | 0.81 (0.32, 2.03) | 0.99 (0.79, 1.23) | 1.18 (0.59, 2.35) |
| Separated/divorced/widowed | 0.66 (0.27, 1.65) | 1.08 (0.84, 1.37) | 0.64 (0.31, 1.33) |
| Highest educational attainment | |||
| High school (and equivalent) or less | Ref. | Ref. | Ref. |
| Some college (including vocational training or associate’s degree) | 1.76 (0.25, 12.56) | 0.86 (0.68, 1.10) | 0.46* (0.25, 0.84) |
| Bachelor’s degree or more | 1.79 (0.28, 11.62) | 0.79 (0.61, 1.03) | 0.38 (0.15, 1.02) |
| Other | NC | 0.60 (0.14, 2.54) | NC |
| Household size | |||
| 1 | Ref. | Ref. | Ref. |
| 2 | 1.91 (0.86, 4.26) | 0.99 (0.81, 1.20) | 2.87* (1.26, 6.51) |
| 3+ | 2.55 (0.92, 7.10) | 0.62* (0.40, 0.98) | 1.49 (0.57, 3.87) |
| Insurance status | |||
| Insured | NC | Ref. | NC |
| Uninsured | NC | 1.28 (0.99, 1.66) | NC |
| Health characteristics | |||
| Ever diagnosed with precancer (Ref.: No) | 1.31 (0.40, 4.30) | 1.37*** (1.15, 1.64) | 0.32 (0.08, 1.25) |
| Smoked at least 100 cigarettes (Ref.: No) | 0.85 (0.36, 2.01) | 1.14 (0.93, 1.41) | 0.83 (0.47, 1.49) |
| Used illegal substances in the past year (Ref.: No) | 0.91 (0.39, 2.10) | 1.13 (0.93, 1.37) | 0.85 (0.44, 1.65) |
| Number of comorbidities (out of 7) | |||
| 0 | Ref. | Ref. | Ref. |
| 1 | 0.52 (0.19, 1.38) | 1.23 (0.84, 1.81) | 0.54 (0.12, 2.42) |
| 2 | 0.88 (0.26, 3.03) | 1.26 (0.86, 1.86) | 1.24 (0.49, 3.13) |
| 3+ | 0.80 (0.30, 2.10) | 1.51* (1.07, 2.14) | 1.47 (0.59, 3.64) |
| Health system experiences | |||
| How much can you depend on your doctors and other health professionals to give you the care you need? | |||
| Not at all/not very much/somewhat | NC | Ref. | Ref. |
| A lot/a great deal | NC | 1.26 (0.89, 1.78) | 1.54 (0.64, 3.68) |
| Patient–provider communication, mean scoreb | 0.52 (0.21, 1.29) | 1.10 (0.93, 1.30) | 1.00 (0.68, 1.47) |
| Healthcare system distrust, mean scoreb | 1.45 (0.89, 2.36) | 0.89 (0.78, 1.01) | 1.28 (0.99, 1.65) |
| HIV stigma | |||
| Overall HIV stigma, mean scoreb | – | 1.03 (0.88, 1.20) | 1.19 (0.74, 1.93) |
| Personalized stigma, mean scoreb | – | 1.07 (0.94, 1.21) | 1.27 (0.86, 1.88) |
| Disclosure concerns, mean scoreb | – | 1.01 (0.90, 1.13) | 0.86 (0.58, 1.26) |
| Concerns with public attitudes, mean scoreb | – | 1.06 (0.93, 1.22) | 1.01 (0.68, 1.52) |
| Negative self-image, mean scoreb | – | 0.96 (0.86, 1.07) | 1.20 (0.86, 1.69) |
| Number of participants eligible for screening | 46 | 293 | 73 |
Bolded values indicate statistical significance
NC not computable
*p<0.05, **p<0.01, ***p<0.001
aAdjusted prevalence ratios were computed using Poisson regressions with log-link function and robust standard errors. The outcome was regressed on each characteristic independently. All models were adjusted for age (years) and race/ethnicity, stratified by sex at birth and HIV status. Missing categorical independent variables were included in the regression as a separate category but were not shown for brevity
bParticipants with >20% of items missing on the scale were excluded
Among women eligible for cervical cancer screening, 60.0% had received guideline-adherent cervical screening (46.6% of WWH and 71.1% of WWoH; p<0.001). WWH were less likely to receive guideline-adherent cervical cancer screening compared to WWoH (aPR 0.60, 95% CI 0.47, 0.77, Table 4). Among WWH, having greater HIV-related disclosure concerns was associated with lower cervical cancer screening uptake (aPR 0.75, 95% CI 0.60, 0.94). WWH of NH-other races were more likely to receive cervical cancer screening compared to NH-White WWH (aPR 1.84, 95% CI 1.02, 3.31).
Table 4.
Adjusted associations of sociodemographic, health, and social predictors with guideline-adherent cervical cancer screening uptake among screening-eligible women
| Characteristics | aPR (95% CI)a |
|---|---|
| Living with HIV | |
| No | Ref. |
| Yes | 0.60*** (0.47, 0.77) |
| Women without HIV | Women with HIV | |
|---|---|---|
| Sociodemographic | ||
| Age (years) | 1.01 (1.00, 1.02) | 1.00 (0.98, 1.02) |
| Race/ethnicity | ||
| White, non-Hispanic | Ref. | Ref. |
| Black, non-Hispanic | 1.22 (0.93, 1.60) | 1.13 (0.68, 1.87) |
| Hispanic/Latino | 0.97 (0.68, 1.38) | 1.05 (0.56, 1.99) |
| Other, non-Hispanic | 1.14 (0.78, 1.67) | 1.84* (1.02, 3.31) |
| Sexual orientation | ||
| Straight | Ref. | Ref. |
| Lesbian or gay | 0.53 (0.19, 1.47) | NC |
| Bisexual | 0.76 (0.54, 1.08) | 0.71 (0.33, 1.52) |
| Other | 0.83 (0.41, 1.68) | 0.74 (0.16, 3.38) |
| Marital status | ||
| Never married | Ref. | Ref. |
| Now married | 1.40** (1.11, 1.75) | 0.67 (0.34, 1.33) |
| Separated/divorced/widowed | 1.18 (0.90, 1.55) | 1.06 (0.66, 1.69) |
| Highest educational attainment | ||
| High school (and equivalent) or less | Ref. | Ref. |
| Some college (including vocational training or associate’s degree) | 1.01 (0.79, 1.30) | 1.22 (0.76, 1.96) |
| Bachelor’s degree or more | 1.10 (0.83, 1.45) | 1.05 (0.53, 2.10) |
| Household size | ||
| 1 | Ref. | Ref. |
| 2 | 0.96 (0.67, 1.38) | 1.22 (0.67, 2.20) |
| 3+ | 1.29 (0.99, 1.68) | 1.07 (0.64, 1.80) |
| Insurance status | ||
| Insured | Ref. | NC |
| Uninsured | 0.78 (0.50, 1.23) | NC |
| Health characteristics | ||
| Ever diagnosed with precancer (Ref.: No) | 1.13 (0.79, 1.62) | 1.61 (0.90, 2.88) |
| Smoked at least 100 cigarettes (Ref.: No) | 1.30* (1.05, 1.60) | 1.10 (0.73, 1.65) |
| Used illegal substances in the past year (Ref.: No) | 0.76* (0.60, 0.95) | 0.90 (0.59, 1.39) |
| Number of comorbidities (out of 7) | ||
| 0 | Ref. | Ref. |
| 1 | 1.28 (0.96, 1.71) | 0.64 (0.35, 1.18) |
| 2 | 1.51** (1.16, 1.97) | 0.97 (0.56, 1.68) |
| 3+ | 1.17 (0.73, 1.88) | 0.97 (0.54, 1.75) |
| Health system experiences | ||
| How much can you depend on your doctors and other health professionals to give you the care you need? | ||
| Not at all/not very much/somewhat | Ref. | Ref. |
| A lot/a great deal | 1.29 (0.95, 1.74) | 1.33 (0.71, 2.50) |
| Patient–provider communication, mean scoreb | 1.05 (0.91, 1.20) | 1.09 (0.84, 1.43) |
| Healthcare system distrust, mean scoreb | 1.00 (0.89, 1.12) | 0.95 (0.75, 1.20) |
| HIV stigma | ||
| Overall HIV stigma, mean scoreb | 0.76 (0.51, 1.15) | 0.77 (0.57, 1.03) |
| Personalized stigma, mean scoreb | 0.89 (0.62, 1.29) | 0.84 (0.65, 1.09) |
| Disclosure concerns, mean scoreb | 0.75 (0.56, 1.01) | 0.75* (0.60, 0.94) |
| Concerns with public attitudes, mean scoreb | 0.77 (0.54, 1.09) | 0.84 (0.65, 1.08) |
| Negative self-image, mean scoreb | 0.96 (0.71, 1.30) | 0.88 (0.72, 1.08) |
| Number of participants eligible for screening | 166 | 128 |
Bolded values indicate statistical significance
NC not computable
*p<0.05, **p<0.01, ***p<0.001
aAdjusted prevalence ratios were computed using Poisson regressions with log-link function and robust standard errors. The outcome was regressed on each characteristic independently. All models were adjusted for age (years) and race/ethnicity, stratified by age group and HIV status. Missing categorical independent variables were included in the regression as a separate category but were not shown for brevity
bParticipants with >20% of items missing on the scale were excluded
Discussion
We aimed to identify predictors of anal and cervical cancer screening uptake among adults with and without HIV receiving care at a community-based health clinic network. Our findings showed that MWH were more likely to have ever been screened for anal cancer compared to MWoH. These findings provide evidence that tailored anal cancer screening guidelines for PWH and men who have sex with men are crucial for increasing anal cancer screening uptake among high-risk and sexual minority populations who have traditionally underutilized other cancer screenings [29]. The providers at CAN Community Health are also highly attuned to the unique needs of sexual and racial/ethnic minorities that seek care at CAN, and they deliver integrated social services that connect their patients to other health-related social needs. Community-based and culturally sensitive cancer screening programs have been shown to improve screening uptake among underserved and minority communities [30].
Several factors were associated with anal cancer screening uptake among our study population. Higher anal cancer screening use among individuals with greater comorbidity burden or any precancer diagnosis is consistent with evidence that individuals who experience more frequent medical encounters are more likely to receive recommended preventive services [31]. In contrast, lower anal cancer screening uptake among participants living in larger households may reflect social or structural barriers, such as competing caregiving responsibilities, reduced ability to attend preventive visits, or limited socioeconomic means, which are patterns documented in the broader cancer prevention and HIV behavioral literature [32]. We additionally found that MWH of NH-other races were more likely to undergo anal cancer screening compared to NH-White MWH, aligning with prior studies reporting differences in anal cancer screening uptake by race/ethnicity [33]. Consistent with prior studies, women in our study had a lower crude prevalence of anal cancer screening than men (41.5% vs. 63.2%), which is an important finding given the rising rates of advanced-stage anal cancer and higher anal cancer-related mortality among women [34]. Collectively, these results underscore the need for targeted, population-specific strategies to reduce disparities in anal cancer screening and to ensure equitable access to prevention services.
In our study population, only 47% of WWH (compared to 71% of WWoH) had received guideline-adherent cervical cancer screening, even though U.S. guidelines recommend more frequent cervical cancer screening in this population [35]. These findings can help clinicians to identify at-risk populations for targeted cervical cancer screening efforts. Specific barriers to receipt of cervical cancer screening include limited knowledge, low awareness of screening guidelines, stigma associated with discussing sexual health, and gap in provider knowledge and training [36–38]. For PWH, these barriers are often compounded by factors such as competing health priorities, fragmented care, HIV stigma, and adverse structural factors such as transportation barriers or unstable housing [39–41]. Previous studies have found that discrimination, medical mistrust, and stigma are barriers to receipt of cancer preventive services [42]. In our study, greater stigma related to concerns about HIV status disclosure was associated with lower cervical cancer screening uptake, reinforcing a growing body of qualitative and quantitative evidence showing that stigma undermines preventive behaviors, engagement in care, and trust in medical systems among PWH [42]. Together, these findings highlight the need for multilevel interventions—particularly those addressing psychosocial stigma, sexual orientation-specific needs, and structural barriers—to improve equitable uptake of anal and cervical cancer screening across populations living with HIV.
Social determinants of health also significantly impact cancer incidence, cancer preventive behaviors, stage at diagnosis, and survival among PWH [10, 43–47]. To address the structural barriers and disparities in cancer screening, targeted interventions are needed. Ensuring that clinicians are aware of evidence-based guidelines and cancer prevention options, trained in recommended procedures, and equipped to address structural and psychosocial barriers will be essential for improving screening equity. Strategies to increase cervical cancer screening uptake, including education campaigns, promotion through mass media, and enhanced reminders, have shown promise [48, 49]. Self-collection kits can expand HPV testing and overcome barriers such as geographic inaccessibility, inadequate health care access or resources, and stigma of pelvic examinations [50, 51]. Our findings identified key populations who may require additional support to fully benefit from advancements in cancer prevention.
Limitations
Our findings should be considered in light of the following limitations. First, this study was conducted at a health clinic network predominantly based in Florida with high engagement of diverse patients. Our findings may not be generalizable to other clinics more broadly. The patient demographic at CAN, including among PWoH, tended to be more racially and ethnically diverse with more sexual minority patients compared to the general population [17]. Additional studies are needed to validate and compare these findings with other healthcare settings. Second, our survey only captured patient characteristics and patient-reported outcomes. Future work should explore provider and clinical characteristics that may be associated with anal and cervical cancer screening, including provider knowledge and engagement in shared decision-making about screening recommendations. Third, due to limitations in the survey, this study was only able to examine the use of cervical Pap test and not high-risk HPV testing in determining guideline-adherent cervical cancer screening. Fourth, the cross-sectional nature of the study design precludes causal inference, and the temporal relationship between associations (for example, a precancer diagnosis and anal or cervical cancer screening) cannot be established. Fifth, small sample sizes in certain stratified models may limit the statistical power and interpretability of findings.
Conclusion
Our findings showed that MWH were more likely than MWoH to receive any anal cancer screening while WWH were less likely than WWoH to receive guideline-adherent cervical cancer screening. Among PWH, screening uptake differed by characteristics, including race/ethnicity, household size, any precancer diagnosis, comorbidities, and HIV-related stigma. Our findings can be used to inform targeted interventions for early anal and cervical cancer detection to improve patient quality of life, morbidity, and mortality. Future work should examine patient outcomes downstream of cancer screening among PWH, including follow-up for abnormal test results, treatment receipt, and survival.
Author contributions
Yu Chen Lin contributed to methodology; formal analysis; writing—original draft. Emma Hume contributed to project administration; writing—review & editing. Carol Boxtha contributed to project administration; writing—review & editing. Sarah A. Commaroto contributed to writing—original draft. Morgan Lael contributed to project administration; writing—review & editing. Shannon M. Christy contributed to methodology; writing—review & editing. Susan T. Vadaparampil contributed to methodology; writing—review & editing. Anna R. Giuliano contributed to methodology; writing—review & editing. Anna E. Coghill contributed to methodology; writing—review & editing. Matthew B. Schabath contributed to methodology; writing—review & editing. Damon J. Vidrine contributed to methodology; writing—review & editing. Jasmine Peterson contributed to conceptualization; methodology; project administration; writing—review & editing. Shannon DiPalmo contributed to conceptualization; methodology; project administration; writing—review & editing. Hemali Joshi contributed to conceptualization; methodology; writing—review & editing. Prerak Shukla contributed to conceptualization; methodology; supervision; project administration; writing—review & editing. Jennifer I. Vidrine contributed to conceptualization; methodology; formal analysis; supervision; project administration; funding acquisition; writing—review & editing. Jessica Y. Islam contributed to conceptualization; methodology; formal analysis; supervision; project administration; writing—review & editing.
Funding
This study was supported by Moffitt Cancer Center’s Office of Community Outreach and Engagement.
Data availability
The datasets used and/or analyzed in this study are available from the corresponding author on reasonable request.
Declarations
Conflict of interest
All authors have no competing interests to disclose.
Ethical approval
This study was reviewed and deemed exempt by Moffitt’s Institutional Review Board of Record, Advarra (Pro00077872).
Informed consent
Informed consent was obtained from all participants.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets used and/or analyzed in this study are available from the corresponding author on reasonable request.