Health care provider characteristics associated with anal cancer screening in an urban academic medical system in the United States

Abstract

Background

New guidelines recommend anal cancer screening for priority populations with increased likelihoods of anal cancer including people with a history of HIV, gynecologic cancers, condyloma acuminata, and solid organ transplantation. However, little is known about U.S.-based screening practices prior to these guidelines.

Methods

We examined outpatient clinical encounters between 01/01/2015 and 08/01/2022 and analyzed provider characteristics and screening behaviors in an urban medical system in Boston, U.S. We used chi-squared tests and logistic regression to identify provider factors associated with anal cancer screening.

Results

Of 1098 providers, 48.5% completed at least one screening, including 93.8% (n = 75/80) of infectious disease (ID) providers, 54.6% (n = 372/681) of primary care providers (PCPs), and 28.3% (n = 41/145) of obstetrician/gynecologists (OBGYNs) (p < 0.001). Annual screening of priority populations was most common among providers trained in high-resolution anoscopy (19.8%–27.9% screened), and less common among ID providers (4.4%–8.7%), PCPs (0.4%–1.4%), and OBGYNs (0.1%–0.8%). In multivariate analysis, providers treating proportionately more cisgender women (adjusted odds ratio [aOR] = 0.988; 95% confidence interval [CI] 0.982–0.995), more non-white patients (aOR = 0.984; 95% CI 0.976–0.992), or fewer people with HIV were less likely to be screeners.

Conclusions

Most providers caring for priority populations did not complete anal cancer screenings, and annual screening levels were low across disciplines. Strategies are needed to optimize anal cancer screening practices, particularly for patients who are HIV-negative, non-white, and cisgender women.

Keywords

Anal cytology anal cancer anal neoplasia men who have sex with men high-resolution anoscopy HIV human papillomavirus organ transplant

Introduction

Anal cancer remains a health concern in the United States, with an estimated 9760 new diagnoses in 2023.¹ Anal cancer disproportionately affects people with HIV (PWH),^2–8 men who have sex with men (MSM),^4–6,8 and individuals with a history of condyloma acuminata,^2,9 solid organ transplantation,^3,5,6,8 human papillomavirus (HPV) mediated gynecologic cancers,^5,6,8 and autoimmune conditions.^2,3,5,8 Screening for anal cancer can be completed through digital anal rectal exams (DARE)^10,11 and anal cytology testing,^10,12–14 where anal canal cells are sampled with moistened polyester swabs and evaluated for signs of cellular dysplasia.^12–14 Co-testing for oncogenic HPV strains may be performed alongside anal cytology,¹⁰ although there is no consensus on its clinical use in this context,^8,15,16 and some recommendations discourage its use.¹⁷ Patients found to have dysplastic anal cytology results are referred for high resolution anoscopy (HRA), if available, where concerning lesions may be treated with excisional or ablative procedures.^8,18–21 A recent study found that HRA decreased anal cancer incidence by 57% among PWH with high-grade anal dysplasia,²² suggesting benefits to anal cancer screening in PWH and potentially additional populations.

Despite possible benefits, several barriers likely limit uptake of anal cancer screening. Anal cytology testing has lower specificity and potentially sensitivity than cervical cytology testing,^16,23 which may dissuade providers from screening, and HRA is not accessible for many patients due to the lack of HRA-trained providers,²⁴ in which case screening is not recommended. While international guidelines on HRA competencies were introduced in the mid-2010s,²¹ and regional and expert guidance on anal cytology screening have progressively developed for populations including PWH,^8,10,25,26 MSM,^10,21,26 individuals with a history of condyloma acuminata,^10,25 solid organ transplantation,^10,27 and HPV-associated gynecologic cancers,^10,22 no national or international screening guidelines were available until January, 2024.¹⁰ Provider comfort in performing anal cytology testing and triaging results remains low,^11,28 yet little is otherwise known about providers’ actual anal cancer screening practices.

The goal of this study was to examine provider screening behaviors and characteristics associated with anal cancer screening in an urban, U.S.-based tertiary-care, academic medical system with HRA access prior to the issuance of international guidelines. We aimed to identify disparities in anal cancer screening to recognize providers that could benefit from training, workflow assistance, and other resources in pursuit of equitable anal cancer prevention.

Methods

Study population

We analyzed electronic medical record (EMR) data from an academic medical center in Boston, U.S., and its two affiliated community clinics with a shared EMR system. All three health centers possessed anal cytology and HPV co-testing capabilities as well as HRA access via two in-house HRA practitioners or referrals to a fourth health facility offering HRA.

Our study population included all physicians and advanced practice providers in departments that completed at least one anal cytology screening between January 1, 2015 and August 1, 2022 including primary care providers (PCPs), infectious disease (ID) specialists, obstetrician/gynecologists (OBGYNs), oncologists, gastroenterologists, transplant surgeons, and urologists. Providers fit inclusion criteria if they worked in an eligible department and treated at least one priority patient within their patient panel.

Priority patients were defined as adult patients who either: (1) had a history of HIV, condyloma acuminata, HPV-associated gynecologic (cervical, vulvar, or vaginal) cancers, or solid organ transplantation identified through ICD-9 or 10 codes, or (2) self-identified as transgender (transgender, gender-non-conforming, non-binary), or as gay, bisexual, queer, pansexual, or questioning men in the EMR. We only included priority patients who were retained in care, which we defined as having two or more ambulatory care visits in the same eligible clinical department within a 5-year period. We used a 5-year period to capture more screening events, given the expectation that time intervals between the first and subsequent screenings would vary in the absence of standardized practices. Patients diagnosed with anorectal squamous cell carcinoma (identified through ICD-9 and 10 codes) prior to study onset were excluded.

We extracted outpatient clinical data on providers’ anal cytology screening and HPV co-testing practices during the study period among priority patients actively retained in care. Based on these data, we classified providers as “screeners” if they screened at least one priority patient with anal cytology and “never-screeners” if they screened no patients. We further classified screeners as “HPV co-testers” if they co-tested at least one patient for E6/E7 mRNA or DNA from high-risk HPV strains during anal cytology screening and “never HPV co-testers” if they had not co-tested any patients. We did not evaluate provider DARE or HRA referral practices as these data were not systematically documented in the EMR. This study was deemed exempt by the Beth Israel Deaconess Medical Center institutional review board.

Outcomes

Our primary outcomes were the number of providers who were anal cytology screeners and HPV co-testers as well as the provider factors associated with these behaviors. Secondary outcomes included: (1) providers’ annual proportion of priority patients screened with anal cytology, and (2) providers’ annual proportion of patients rescreened with anal cytology after an initial negative cytology screen.

Covariates

Provider characteristics used as covariates included provider specialty (ID specialists, OBGYNs, PCPs, or other), HRA training (HRA provider vs non-HRA-provider), and practice site (academic center, community sites, or both). We also quantified variability in providers’ patient panels with respect to important patient characteristics. First, we calculated the median patient age in each provider’s panel and the percentage of patients in that panel who were non-White, Hispanic, cisgender women, transgender, unknown gender, or covered by public insurance. Next, we determined the median value for each of these variables across all providers. We subsequently calculated the difference between each provider’s panel and the median value across all providers for each of these variables, and these differences represented covariates for our main analyses. We also developed a categorical variable describing the volume of PWH in each provider’s panel (0, 1–9, 10–49, 50+ patients).

Statistical analysis

We used descriptive statistics to characterize screenings among all providers and stratified by whether providers were screeners and, separately, whether screeners were HPV co-testers. Differences were tested using chi-squared tests or Wilcoxon rank sum tests for non-normally distributed variables. We also calculated yearly trends in the proportion of priority patients that were screened and stratified these trends by provider specialty, practice site, and patients’ prior anal cytology screening results.

We used multivariable logistic regression with robust standard errors to analyze whether provider screening was associated with provider or patient panel characteristics, and adjusted for all the above covariates. We reported adjusted odds ratios (aORs) with 95% confidence intervals (CIs). We did not perform multivariable regression on HPV co-testing practices due to small numbers of co-testers. Analyses were performed using Stata SE (version 16.1, StataCorp) and were two-tailed, with p-values <0.05 considered statistically significant.

Results

Anal cytology screening

Of 1098 providers in the study cohort, who together had 7654 priority patients on their patient panels, 48.5% (n = 533) were anal cytology screeners (Table 1). Screening practices varied by provider specialty and panel composition with respect to age, gender, and number of PWH. ID specialists were most likely to be screeners among all medical specialties: 93.8% (n = 75/80) were screeners compared with 54.6% (n = 372/681) of PCPs, 28.3% (n = 41/145) of OBGYNs and 23.4% (n = 45/192) of all other eligible providers (oncologists, gastroenterologists, transplant surgeons, urologists) (p < 0.001). Screeners’ priority population panels had a median age of 53.5 years (interquartile range [IQR] 49.0–57.0) compared with 52.0 (IQR 41.0–59.0) for never-screeners (p < 0.001). Screeners’ panels had proportionately more cisgender men than never screeners (median 46.2% [IQR 26.1–62.1] vs median 28.6% [IQR of 0.0%–53.3%]; p < 0.001) and proportionately fewer cisgender women (median 52.6% IQR 37.5%–73.7%] vs median 71.4% [IQR 46.2%–100%]; p < 0.001). With respect to PWH, 3.6% (n = 7/193) of providers with 0 PWH, 43.3% (n = 263/607) with 1–9 PWH, 86.2% (n = 200/232) with 10–49 PWH, and 95.5% (n = 63/66) with 50+ PWH were screeners (p < 0.001). Provider screening was not associated with clinical site or the racial, ethnic, or insurance composition of patient panels.

Table 1.

Anal cytology (AC) screening and human papillomavirus (HPV) co-testing by provider characteristics.

	Overall		Never AC screening providers		AC screening providers			Never HPV co-testing providers		HPV co-testing providers		p-value
	n / median	% / (IQR)	n / median	% / (IQR)	n / median	% / (IQR)	p-value	n / median	% / (IQR)	n / median	% / (IQR)	p-value
Total providers	1098	100.00%	565	51.46%	533	48.54%		492	92.31%	41	7.7%
Specialty, n %							<0.001					<0.001
Infectious disease	80	7.29%	5	6.25%	75	93.75%		67	89.33%	8	10.7%
OBGYN⁺	145	13.21%	104	71.72%	41	28.28%		28	68.29%	13	31.7%
Primary care	681	62.02%	309	45.37%	372	54.63%		352	94.62%	20	5.4%
Other^#	192	17.49%	147	76.56%	45	23.44%		45	100.00%	0	0.0%
Clinical site, n %							0.95					0.78
Academic center	970	88.34%	498	51.34%	472	48.66%		437	92.58%	35	7.4%
Community sites	89	8.11%	46	51.69%	43	48.31%		29	67.44%	4	9.3%
Academic & community sites	39	3.55%	21	53.85%	18	46.15%		16	88.89%	2	11.1%
Age, median years of patient panel (IQR^)							<0.001					0.007
Age	53	(45.5–58)	52.0	(41.0–59.0)	53.5	(49.0–57.0)		53.5	(49.0–57.0)	52.0	(43.0–56.0)
Race, median % of patient panel (IQR^)
White	53.0	(38.5–68.2)	50.0	(33.3–75)	54.4	(42.9–66.2)	0.44	54.6	(42.9–66.3)	52.1	(46.3–63.7)	0.41
Unknown	0.0	(0–2.6)	0.0	(0–0)	0.0	(0–3.6)		0.0	(0–3.5)	2.2	(1–4.8)
Non-white	43.9	(28.4–60)	45.0	(23.7–66.7)	43.5	(32.1–54.1)	0.46	42.9	(31.8–55.2)	45.9	(33.3–51.8)	0.51
Asian	0.0	(0–6.3)	0.0	(0–6.3)	1.9	(0–6.3)	0.11	1.6	(0–6.3)	3.2	(1.4–6.7)	0.62
Black	31.3	(15–46.5)	30.0	(9.5–50)	32.8	(20.8–42.3)	0.55	31.7	(20.1–42.4)	35.3	(26.3–42.3)	0.33
American indian	0.0	(0–0)	0.0	(0–0)	0.0	(0–0)		0.0	(0–0)	0.0	(0–0.3)
Other	3.6	(0–10)	0.0	(0–9.1)	5.6	(0–10.5)	0.19	5.6	(0–10.6)	4.8	(3.8–7.6)	0.47
Ethnicity, median % of patient panel (IQR^)
Hispanic	11.1	(0–19.2)	7.7	(0–20)	12.5	(7.1–18.8)	0.09	12.5	(6.9–18.9)	14.3	(9.9–18.5)	0.64
Non-hispanic	88.9	(80.5–100)	92.3	(80–100)	87.5	(81–92.9)	0.08	87.5	(81–93)	85.7	(81.5–90.1)	0.66
Unknown	0.0	(0–0)	0.0	(0–0)	0.0	(0–0)		0.0	(0–0)	0.0	(0–0)
Gender, median % of patient panel (IQR^)
Cis-men	39.1	(12.3 – 60.0)	28.6	(0–53.3)	46.2	(26.1–62.1)	<0.001	47.1	(27.9–62.5)	33.4	(0 – 56.0)	0.001
Cis-women	60.0	(40,0–87.5)	71.4	(46.2–100)	52.6	(37.5–73.7)	<0.001	52.4	(37.4–71.4)	66.6	(43.7–98.9)	0.002
Transgender	0.0	(0–0)	0.0	(0–0)	0.0	(0–0)		0.0	(0–0)	0.0	(0–0.8)
Gender identity unknown	0.0	(0–0)	0.0	(0–0)	0.0	(0–0)		0.0	(0–0)	0.0	(0–0)
Insurance, median % of patient panel (IQR^)
Private	30.0	(17.7–42.7)	27.3	(10.8–46.7)	31.3	(21.9–40)	0.81	30.8	(21.1–39.1)	37.0	(30.6–43.9)	0.003
Public	66.7	(53.9–78.3)	66.7	(50–83.3)	66.7	(57.1–75)	0.59	66.7	(57.3 – 75.0)	60.0	(52.6–68.8)	0.005
Other	0.0	(0–4.4)	0.0	(0–3.8)	1.4	(0–4.7)	0.04	1.0	(0–4.8)	2.5	(0.4–3.6)	0.59
Number of PWH* in patient panel, n %							<0.001					<0.001
0	193	17.58%	186	96.37%	7	3.63%		7	100.00%	0	0.0%
1 to 9	607	55.28%	344	56.67%	263	43.33%		254	96.58%	9	3.4%
10 to 49	232	21.13%	32	13.79%	200	86.21%		186	93.00%	14	7.0%
50 +	66	6.01%	3	4.55%	63	95.45%		45	71.43%	18	28.6%
% HIV, median (IQR)	23.8	(8–41.2)	15.0	(0–33.3)	33.0	(20–50)		33.2	(20–50)	27.3	(16.7–75)	0.49

AC = Anal Cytology.

IQR^ = Interquartile Range.

OBGYN⁺ = Obstetrician/ Gynecologist.

Other^# = includes oncologists, transplant surgeons, gastroenterologists, and urologists.

PWH = People with HIV.

In multivariate analyses, provider screening was associated with provider specialty and panel composition with respect to race, gender, and number of PWH (Table 2). PCPs were 64.0% less likely to be screeners than ID specialists (aOR = 0.360; 95% CI 0.130–0.997). Providers in other eligible specialties were 95.6% less likely to be screeners than ID specialists (aOR = 0.044; 95% CI 0.015–0.131). Providers treating a higher proportion of non-white patients (aOR = 0.984; 95% CI 0.976–0.992) or cisgender women (aOR = 0.988; 95% CI 0.982–0.995) were statistically less likely to be screeners. Providers had 20 times greater odds of screening if they had 1–9 PWH (aOR = 20.212; 95% CI 8.912–45.842), 159 times greater with 10–49 PWH (aOR = 158.839; % CI 64.559–390.802), and 453 times greater with 50+ PWH in their panels (aOR = 453.055; 95% CI 115.320–1779.897). Provider screening was not associated with clinical site or the age, ethnic, or insurance composition of patient panels.

Table 2.

Anal cytology screening by provider characteristics (multivariate logistic regression).

Provider characteristics	Screening providers
Specialty	Odds ratio(95% Confidence Interval)	p-Value
Infectious disease	Base group -	Base group -
Obstetrics/Gynecology	0.35724(0.10944,1.16617)	0.09
Primary care	0.35985*(0.12984,0.99733)	0.049
Other⁺	0.04421*(0.01489,0.13128)	<0.001
Clinical site
Academic center	Base group -	Base group -
Community sites	0.98963(0.51223,1.91199)	0.98
Academic & community sites	1.21744(0.60060,2.46779)	0.59
Age composition of patient panel (year difference from median)
Age	1.0188(0.99687,1.04120)	0.09
Race/Ethnicity composition of patient panel (percentage point difference from median)
Non-white	0.98414*(0.97683,0.99151)	<0.001
Hispanic	1.00661(0.99558,1.01775)	0.24
Gender composition of patient panel (percentage point difference from median)
Cisgender women	0.98841*(0.98148,0.99538)	0.001
Transgender	1.0405(0.95503,1.13362)	0.36
Unknown gender	1.58293(0.66809,3.75053)	0.30
Insurance composition of patient panel (percentage point difference from median)
Public insurance	1.00136(0.99310,1.00970)	0.75
Number of PWH^ in patient panel
0	Base group -	Base group -
1 to 9	20.21226*(8.91174,45.84239)	<0.001
10 to 49	158.83851*(64.55866,390.80227)	<0.001
50 +	453.05464*(115.32042,1779.89729)	<0.001

*= Denotes statistical significance with affiliated 95% confidence intervals that do not cross zero.

Other⁺ = includes oncologists, transplant surgeons, gastroenterologists, and urologists.

PWH^ = People with HIV.

The proportion of priority patients annually screened for anal cytology varied by provider HRA expertise and specialty. Among patients who both: (1) had at least one appointment during the year with a provider included in the study, and (2) did not already have anal cytology results documented within the year, HRA-trained providers (which included 1 PCP and 1 ID specialist) annually screened 19.8%–27.9% of their priority patients, while non-HRA-trained ID specialists screened 4.4%–8.7%, PCPs screened 0.4%–1.4%, OBGYNs screened 0.1%–0.8%, and “other” providers screened 0.0%–0.2% (Figure 1). Annual screening decreased for HRA-trained providers and ID specialists in 2020, coinciding with the COVID-19 pandemic, but increased in 2021 before decreasing in 2022 to below pre-pandemic levels. Screening remained low and did not significantly change during this period for all other providers.

Figure 1.

Mean proportion of priority patients with ambulatory care visits screened with anal cytology by year and provider specialty.

Providers who worked exclusively at the academic medical center annually screened 2.4%–3.6% of their priority patients compared with 0.0%–0.7% for providers exclusively at community sites and 0.0%–1.1% for those at both academic and community sites (Figure 2). Annual screenings decreased in 2020 among providers working at either academic or community sites, increased in 2021, and decreased again in 2022. Annual screenings among providers working at both academic and community sites remained at 0.0% from 2019 to 2021, but increased to 1.1% in 2022.

Figure 2.

Mean proportion of priority patients with ambulatory care visits screened with anal cytology by year and clinical site.

Among screening providers with at least one patient with an initial non-dysplastic (i.e., normal) anal cytology screening result, 100% (n = 2/2) of HRA-trained providers rescreened 32.4% (n = 33/102) of their patients within 1 year and 51.0% (52/102) within 6 years, 41.7% (n = 15/36) of ID specialists respectively rescreened 16.2% (n = 17/105) and 31.4% (n = 33/105) of their patients, and 100% (n = 2/2) of PCPs rescreened 3.7% (n = 3/81) and 9.9% (n = 8/81); 14.3% (n = 1/7) of OBGYNs rescreened 7.7% (n = 1/13) within 1–2 years, and 11.4% (n = 5/44) of other providers rescreened 100% (n = 2/2) within 1 year, but longer-term screening practices could not be evaluated for these specialties due to limited durations of follow-up between these providers and their patients (Figure 3).

Figure 3.

Proportion of patients rescreened with anal cytology after an initial non-dysplastic screening by year and clinical specialty.

HPV co-testing

Of the 533 providers who completed anal cytology screening, 7.7% (n = 41/533) completed HPV co-testing at least once (Table 1). Co-testing practices varied by provider specialty and panel composition with respect to age, gender, insurance, and number of PWH. OBYGNs were most likely to be co-testers among all specialties: 31.7% (n = 13/41) were co-testers compared with 10.7% (n = 8/75) of ID specialists, 5.4% (n = 20/372) of PCPs, and 0.0% (n = 0/45) of other providers (p < 0.001). Co-testers’ panels had a median age of 52.0 (IQR 43.0–56.0) compared with 53.5 (IQR 49.0–57.0) for never co-testers (p = 0.007). Co-testers’ panels had proportionately more cisgender women than never co-testers (median 66.6% [IQR 43.7%–98.9%] vs median 52.4% [IQR 37.4%–71.4%]; p = 0.002) and proportionately more privately insured patients than never co-testers (median 37.0% [IQR 30.6%–43.9%] vs median 30.8% [IQR 21.1%–39.1%]; p = 0.003). With respect to PWH, 0.0% (n = 0/7) of providers with 0 PWH, 3.4% (n = 9/263) with 1–9 PWH, 7.0% (n = 14/200) with 10–49 PWH, and 28.6% (n = 18/63) with 50+ PWH were co-testers (p < 0.001). Provider co-testing was not associated with provider clinical site or the racial or ethnic composition of patient panels.

Conclusions

This is a retrospective cohort study of provider anal cancer screening practices in an urban, U.S.-based medical system with HRA access. Our major finding was that the minority (48.5%) of providers who treated patients with higher likelihoods of developing anal cancer completed any anal cancer screening during the nearly 8-year study period. Screeners were most likely to be ID specialists, followed by OBGYNs, PCPs, and finally all other included providers. Apart from HRA-trained providers, few providers across disciplines annually screened priority patients with anal cytology. We also noted screening disparities, as providers with greater proportions of non-white patients, cisgender women, or non-PWH in their panels were less likely to perform screening. Our findings suggest a need to support providers in equitably and routinely screening priority patients for anal cancer across specialties.

In our study, ID specialists were most likely to be anal cytology screeners. This likely reflects larger numbers of PWH in their panels compared to other specialties, which was also independently associated with screening. The relationship between PWH and provider screening is not unexpected, given that expert guidance issued prior to international guidelines recommended screening primarily for PWH^8,10,25,26 or MSM,^10,26,29 and because the ANCHOR²² Trial, a study demonstrating that treating high-grade anal dysplasia with HRA decreases anal cancer incidence, enrolled exclusively PWH. Nonetheless, screening among ID specialists was not universal, suggesting a need to identify strategies that could improve screening practices such educating providers on anal cancer screening, integrating anal cytology screening with existing workflows, and piloting EMR screening prompts for priority patients.

While fewer PCPs and OBGYNs than ID specialists were screeners, these two specialties were more likely to be screeners than other providers in our cohort. This may be due to the relatively higher exposure to PWH than other specialties and that HIV may increasingly be treated by primary care allied disciplines.³⁰ Screening practices were still lower than among ID specialists after controlling for volume of PWH, possibly due to knowledge differences in anal cancer prevention,³⁰ time constraints imposed by patients’ competing medical priorities, or sharing screening responsibilities for PWH with ID colleagues. Other providers including oncologists, transplant surgeons, gastroenterologists, and urologists were least likely to be screeners potentially due to the relative dearth of screening guidance for patients with histories of solid organ transplants and HPV-associated gynecologic cancers until recently.¹⁰ Future studies should explore provider workflows, clinical decision-making, and comfort and knowledge levels for screening within each of these disciplines to improve screening behaviors.

Few providers screened their priority patients annually. HRA-trained providers were most likely to screen patients annually, likely due to performing frequent anal cytology tests on patients referred to them for HRA. ID specialists were next most likely to complete annual screenings, given their high proportions of PWH and MSM patients. Additionally, newer regional²⁹ and international¹⁰ guidelines that provided screening interval recommendations for the priority populations included in our study were not released until after our data collection period, so routine screening may have increased since the completion of our study. Despite the new guidelines, optimal screening intervals are unknown, so additional research to determine optimal intervals could inform guidelines and help standardize practices.

While providers were equally likely to be screeners regardless of provider clinical site, the proportion of priority patients screened annually by providers at the academic medical center was nearly three times higher than in the community sites. This observation could be attributable to variations in provider disciplines and the composition of patient panels across institutions, given that all HRA-trained providers and ID specialists, who tended to have more patients with historically stronger screening indications, were physically located at the academic medical center. It is less likely that providers in the academic health center were more knowledgeable about screening guidelines than community providers, given that the proportion of screening providers was not different across sites. Additional studies to understand how providers in different settings approach screening decisions could further standardize screening practices.

We observed racial and gender screening disparities in our cohort, including that providers with proportionately more non-white patients were less likely to be screeners than those with more white patients. Our observations align with concerning national trends that non-white patients tend to receive age-appropriate cancer screenings at lower rates across medical conditions.^31,32 Given evidence of higher rates of anal dysplasia and cancer among some non-white populations, including Black men,^33,34 additional studies should explore the unique barriers faced by providers in completing anal cytology screenings for priority non-white patients as well as potential implications of reduced screening among these populations. We also found that providers with proportionately more cisgender women were less likely to be screeners than those with more cisgender men. This disparity could be explained by relatively stronger screening recommendations for MSM^10,26,29 and PWH, who are disproportionately men, than for patients with a history of HPV-associated gynecologic cancers.^5,6,8,10 Furthermore, only 17% of the ANCHOR study participants were cisgender women,²² suggesting the need for additional research on the potential benefits of screening among priority cisgender women. Given that nearly 65% of new anal squamous cell cancer diagnoses occur among cisgender women in the U.S.,³⁵ additional research should investigate barriers faced by providers in screening priority cisgender women in order to achieve equitable screening practices.

OBYGNs were most likely to be HPV co-testers of all specialties, potentially due to providers applying strategies from HPV co-testing in cervical cancer screening to anal cytology testing. Given limited data evaluating dual anal cytology screening and HPV co-testing performance,¹⁰ and the lack of consensus over how to utilize HPV co-testing in anal cancer prevention,^8,17 future studies and guidelines should clarify potential benefits and harms to HPV co-testing as well as delineate gold-standard co-testing practices in relation to anal cancer screening.

There were limitations to our study. First, we did not have access to comprehensive provider-level demographic data for the providers in our cohort and were unable to determine associations between those characteristics and screening practices.³⁶ Second, we were unable to examine provider DARE practices or HRA referrals for eligible patients, as none of these factors were consistently documented in the EMR system, and potential HRA sites included providers in allied health centers that used different EMR systems. Finally, our study may have underestimated patients’ screening rates if some priority patients were screened at external sites with separate EMR systems, and our providers appropriately avoided unnecessary screenings for these patients.

In conclusion, our study provides information on providers’ anal cytology screening and HPV co-testing practices among patients with increased likelihoods of developing anal cancer. Our study found that ID providers and those with more PWH, followed by OBGYNs and PCPs, were most likely to be screeners, but that provider screening was low across disciplines. This study also found racial and gender-based screening disparities, such that providers with proportionately more non-white patients or cisgender women were less likely to be screeners. Future studies should investigate screening barriers across specialties and identify unique obstacles in screening cisgender women and non-white patients to ensure equitable screening practices across priority populations.

Footnotes

Acknowledgements

We would like to thank the American Sexually Transmitted Diseases Association (ASTDA) for its provision of a Small Project Assistance grant (DG) as well as the Harvard University Center for AIDS Research for its generous grant funding (P30 AI060354, DK). We would similarly like to thank the Insight Core and the Center for Healthcare Delivery Science at Beth Israel Deaconess Medical Center for their assistance with data extraction and analysis.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This project was funded by the American Sexually Transmitted Diseases Association (ASTDA) for its provision of a Small Grants Award (DG) as well as by Harvard University Center for AIDS Research (P30 AI060354, DK).

Ethical considerations

This study was reviewed and deemed exempt by the Beth Israel Deaconess Medical Center institutional review board on approximately 11/2022.

ORCID iD

Daniel J Gore

Data Availability Statement

Study data will not be shared in a relevant public data repository to protect the privacy of evaluated patient data. However, study data may be provided upon request and on a case-by-case basis if all requests are in-keeping with Harvard University’s ethical and legal considerations.

References

National Cancer Institute . Cancer of the anus, anal canal, and anorectum - cancer stat facts. Cancer Stat Facts: Anal Cancer. https://seer.cancer.gov/statfacts/html/anus.html (accessed 11 April 2024).

Faber

Frederiksen

Palefsky

, et al. A nationwide longitudinal study on risk factors for progression of anal intraepithelial neoplasia grade 3 to anal cancer. Int J Cancer 2022; 151: 1240–1247.

Sunesen

Nørgaard

Thorlacius-Ussing

, et al. Immunosuppressive disorders and risk of anal squamous cell carcinoma: a nationwide cohort study in Denmark, 1978-2005. Int J Cancer 2010; 127: 675–684.

Silverberg

Lau

Justice

, et al. Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clin Infect Dis 2012; 54: 1026–1034.

Clifford

Georges

Shiels

, et al. A meta-analysis of anal cancer incidence by risk group: toward a unified anal cancer risk scale. Int J Cancer 2021; 148: 38–47.

Van der Zee

Richel

De Vries

HJC

, et al.

The increasing incidence of anal cancer: can it be explained by trends in risk groups?

Neth J Med 2013; 71: 401–411.

Machalek

Poynten

Jin

, et al. Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis. Lancet Oncol 2012; 13: 487–500.

Barroso

LFII

Stier

Hillman

, et al. Anal cancer screening and prevention: summary of evidence reviewed for the 2021 centers for disease control and prevention sexually transmitted infection guidelines. Clin Infect Dis 2022; 74: S179–S192.

Nordenvall

Chang

Adami

H-O

, et al. Cancer risk among patients with condylomata acuminata. Int J Cancer 2006; 119: 888–893.

10.

Stier

Clarke

Deshmukh

, et al. International anal Neoplasia Society’s consensus guidelines for anal cancer screening. Int J Cancer 2024; 154: 1694–1702.

11.

Gaydos

Blemur

Perry

, et al. Truth or DARE (digital anal rectal examination): gynecologist viewpoints on anal cancer screening. J Low Genit Tract Dis 2023; 27: 351–355.

12.

Nathan

Singh

Garrett

, et al. Performance of anal cytology in a clinical setting when measured against histology and high-resolution anoscopy findings. AIDS 2010; 24: 373–379.

13.

Cranston

Hart

Gornbein

, et al. The prevalence, and predictive value, of abnormal anal cytology to diagnose anal dysplasia in a population of HIV-positive men who have sex with men. Int J STD AIDS 2007; 18: 77–80.

14.

Palefsky

Holly

Hogeboom

, et al. Anal cytology as a screening tool for anal squamous intraepithelial lesions. J Acquir Immune Defic Syndr Hum Retrovirol 1997; 14: 415–422.

15.

Pernot

Boucheron

Péré

, et al. Comparison of anal cancer screening strategies including standard anoscopy, anal cytology, and HPV genotyping in HIV-positive men who have sex with men. Br J Cancer 2018; 119: 381–386.

16.

Dias Gonçalves Lima

Viset

Leeflang

MMG

, et al. The accuracy of anal swab-based tests to detect high-grade anal intraepithelial neoplasia in HIV-infected patients: a systematic review and meta-analysis. Open Forum Infect Dis 2019; 6: ofz191.

17.

Hazra

Collison

Davis

. CDC sexually transmitted infections treatment guidelines, 2021. JAMA 2022; 327: 870–871.

18.

Cho

Groves

Lao

. History of high-resolution anoscopy. Clin Colon Rectal Surg 2018; 31: 336–346.

19.

Wells

Holstad

Thomas

, et al. An integrative review of guidelines for anal cancer screening in HIV-infected persons. AIDS Patient Care STDS 2014; 28: 350–357.

20.

Pineda

Berry

Jay

, et al. High-resolution anoscopy targeted surgical destruction of anal high-grade squamous intraepithelial lesions: a ten-year experience. Dis Colon Rectum 2008; 51: 829–835.

21.

Hillman

Cuming

Darragh

, et al. 2016 IANS international guidelines for practice standards in the detection of anal cancer precursors. J Low Genit Tract Dis 2016; 20: 283–291.

22.

Palefsky

Lee

Jay

, et al. Treatment of anal high-grade squamous intraepithelial lesions to prevent anal cancer. N Engl J Med 2022; 386: 2273–2282.

23.

Nanda

McCrory

Myers

, et al. Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med 2000; 132: 810–819.

24.

Factor

Cooperstein

Pereira

, et al. Are colon and rectal surgeons ready to screen for anal dysplasia? Results of a survey on attitudes and practice. Sex Transm Dis 2014; 41: 246–253.

25.

Thompson

Horberg

Agwu

, et al. Primary care guidance for persons with human immunodeficiency virus: 2020 update by the HIV Medicine Association of the Infectious Diseases Society of America. Clin Infect Dis 2021; 73: e3572–e3605.

26.

Stewart

Gaertner

Glasgow

, et al. The American Society of Colon and Rectal Surgeons clinical practice guidelines for anal squamous cell cancers (Revised 2018). Dis Colon Rectum 2018; 61: 755–774.

27.

Chin-Hong

Reid

AST Infectious Diseases Community of Practice . Human papillomavirus infection in solid organ transplant recipients: guidelines from the American Society of Transplantation Infectious Diseases Community of Practice. Clin Transplant 2019; 33: e13590.

28.

Sowah

Buchwald

Riedel

, et al. Anal cancer screening in an urban HIV clinic: provider perceptions and practice. J Int Assoc Provid AIDS Care 2015; 14: 497–504.

29.

Hirsch

McGowan

Fine

, et al. Screening for anal dysplasia and cancer in adults with HIV. Report. Baltimore, MD: Johns Hopkins University, 2020.

30.

Wijesinghe

Alexander

. Management and treatment of HIV: are primary care clinicians prepared for their new role? BMC Fam Pract 2020; 21: 130.

31.

Advani

Nayak

, et al. Racial/ethnic disparities in use of surveillance mammogram among breast cancer survivors: a systematic review. J Cancer Surviv 2022; 16: 514–530.

32.

Tsai

M-H

Xirasagar

de Groen

. Persisting racial disparities in colonoscopy screening of persons with a family history of colorectal cancer. J Racial Ethn Health Disparities 2018; 5: 737–746.

33.

Cruz

Chen

Hsu

, et al. Racial and gender disparities in the incidence of anal cancer: analysis of the Nationwide Inpatient Sample (NIS). J Gastrointest Oncol 2019; 10: 37–41.

34.

Walsh

Bertozzi-Villa

Schneider

. Systematic review of racial disparities in human papillomavirus-associated anal dysplasia and anal cancer among men who have sex with men. Am J Public Health 2015; 105: e34–e45.

35.

Deshmukh

Suk

Shiels

, et al. Recent trends in squamous cell carcinoma of the anus incidence and mortality in the United States, 2001-2015. J Natl Cancer Inst 2020; 112: 829–838.

36.

Gagnon

Coulter

RWS

Egan

, et al. Patient and clinician sociodemographics and sexual history screening at a multisite federally qualified health center: a mixed methods study. Ann Fam Med 2023; 21: 395–402.