Abstract
This cross-sectional study evaluates use and availability of follow-up anoscopy among persons at highest risk for anal cancer.
Introduction
Persons with HIV (PWH) in the US are 28 times more likely to be diagnosed with anal cancer than persons without HIV.1 Risk is particularly high among men who have sex with men,2 transgender women,3 and PWH 45 years or older.2 Identifying and treating anal cancer precursors can reduce cancer incidence among PWH.3 For PWH with abnormal cytology results, follow-up high-resolution anoscopy (HRA) is recommended.4 We estimated the number of HRA-eligible PWH at highest risk for anal cancer lacking HRA access because it was not available through their HIV care facility.
Methods
Data were from the 2019 Medical Monitoring Project (MMP), the only US population–based survey of PWH 18 years or older. We also analyzed a 2021 supplemental survey on HRA availability (on-site or by referral) at facilities where 2019 MMP participants received HIV care. Additional information on MMP methods is provided in eAppendix and eMethods in Supplement 1 and elsewhere.5 In accordance with the Common Rule, this cross-sectional study was exempt from ethics review because MMP is a public health surveillance activity. Participants provided oral or written informed consent. We followed the STROBE reporting guideline.
We estimated weighted population frequencies and percentages (with 95% CIs) of PWH eligible for HRA by risk group.4 These PWH at highest risk included (1) gay, bisexual, and other men who have sex with men (GBMSM) or transgender women 35 years or older2,3 and (2) other PWH 45 years or older.2 We examined abnormal anal cytology results (≥atypical squamous cells of undetermined significance [≥ASC-US]) of PWH at highest risk who had cytology during the past 2 years (scenario A). We applied the percentage with abnormal results to estimate the number with abnormal results if all PWH at highest risk had cytology (scenario B) and if all PWH at highest risk who lacked access to HRA on-site or by referral had cytology (scenario C). Analyses accounted for MMP’s complex sample design. Data were analyzed using SAS 9.4 (SAS Institute) and SUDAAN 11.0.3 (RTI International).
Results
Overall, an estimated 31 200 PWH at highest risk for anal cancer (GBMSM or transgender women ≥35 years; other PWH ≥45 years) had abnormal anal cytology results (≥ASC-US) in 2019 (Table). If all PWH at highest risk had cytology and the same distribution of results as those who were actually tested, 422 888 (95% CI, 350 869-494 906) would have had abnormal results. Under the same assumptions, an estimated 124 386 (95% CI, 89 421-159 352) PWH with abnormal results would have no access to follow-up HRA through their HIV care facility.
Table. Estimated Number and Percentage of PWH at Highest Risk for Anal Cancer With Abnormal Cytology Results Who Would Not Have Access to HRAa.
| Cytology results for PWH at highest risk for anal cancerb | No. of MMP participantsc | Weighted population frequency (95% CI) | Cytology result within each group, weighted % (95% CI) | PWH for whom HRA would be recommended, weighted population frequencies (95% CI) | ||||
|---|---|---|---|---|---|---|---|---|
| PWH | PWH seen at facilities without HRA on-site or by referral | Including PWH without cytology | Excluding PWH without cytologyd | Scenario A: PWH who had cytology | Scenario B: if all PWH had cytology | Scenario C: if all PWH seen at facilities without HRA on-site or by referral had cytology | ||
| All PWH at highest riske | 3136 | 787 500 (715 124-859 876) | 231 632 (175 754-287 509) | NA | NA | NA | NA | NA |
| Negative | 119 | NA | NA | 3.4 (2.0-4.9) | 46.3 (38.6-54.0) | NA | NA | NA |
| ≥ASC-US | 130 | NA | NA | 4.0 (2.6-5.4) | 53.7 (46.0-61.4) | 31 200 (18 509-43 891) | 422 888 (350 869-494 906) | 124 386 (89 421-159 352) |
| ASC-US | 68 | NA | NA | 2.2 (1.3-3.0) | 29.1 (23.3-34.9) | 16 903 (9717-24 090) | 229 163 (178 587-279 738) | 67 405 (46 199-88 611) |
| LSIL | 49 | NA | NA | 1.5 (1.0-2.0) | 20.1 (13.4-26.8) | 11 689 (6780-16 598) | 158 288 (103 518-213 057) | 46 558 (27 310-65 806) |
| HSIL, ASC-H, SCC | 13 | NA | NA | 0.3 (0.0-0.7)f | 4.5 (1.3-7.6)f | 2608 (0-5243) | 35 438 (10 419-60 456) | 10 423 (2662-18 185) |
| No cytology | 2861 | NA | NA | 92.6 (89.9-95.2) | NA | NA | NA | NA |
| GBMSM or transgender women aged ≥35 y | 1656 | 426 975 (365 153-488 796) | 122 259 (90 832-153 687) | NA | NA | NA | NA | NA |
| Negative | 88 | NA | NA | 5.0 (3.0-6.9) | 46.3 (38.5-54.1) | NA | NA | NA |
| ≥ASC-US | 102 | NA | NA | 5.8 (3.7-7.9) | 53.7 (45.9-61.5) | 24 308 (13 259-35 358) | 229 286 (182 133-276 439) | 65 653 (46 215-85 091) |
| ASC-US | 52 | NA | NA | 2.9 (1.9-4.0) | 27.2 (21.4-33.0) | 12 325 (6990-17 661) | 116 137 (86 058-146 217) | 33 254 (22 089-44 420) |
| LSIL | 39 | NA | NA | 2.3 (1.3-3.2) | 21.0 (13.5-28.4) | 9489 (4669-14 310) | 89 665 (55 100-124 230) | 25 674 (14 331-37 018) |
| HSIL, ASC-H, SCC | 11 | NA | NA | 0.6 (0.0-1.2)f | 5.5 (1.6-9.4)f | 2494 (0-5124) | 23 484 (6433-40 535) | 6724 (1611-11 837) |
| No cytology | 1445 | NA | NA | 89.2 (85.6-92.9) | NA | NA | NA | NA |
| All other PWH aged ≥45 yg | 1480 | 360 525 (314 211-406 840) | 109 372 (80 268-138 476) | NA | NA | NA | NA | NA |
| Negative | 31 | NA | NA | 1.7 (0.5-2.8)f | 46.3 (29.0-63.5) | NA | NA | NA |
| ≥ASC-US | 28 | NA | NA | 1.9 (0.9-3.0) | 53.7 (36.5-71.0) | 6891 (3412-10 371) | 193 602 (126 593-260 611) | 58 733 (34 124-83 342) |
| ASC-US | 16 | NA | NA | 1.3 (0.4-2.2)f | 35.7 (18.3-53.1) | 4578 (1498-7658) | 128 707 (63 551-193 863) | 39 046 (17 168-60 924) |
| LSIL | 10 | NA | NA | 0.6 (0.2-1.0)f | 17.2 (6.3-28.0)f | 2200 (730-3669) | 62 010 (21 841-102 180) | 18 812 (5784-31 840) |
| HSIL, ASC-H, SCC | 2 | NA | NA | 0.0 (0.0-0.1)f | 0.9 (0.0-2.2)f | 114 (0-271) | 3 245 (0-7942) | 984 (0-2438) |
| No cytology | 1416 | NA | NA | 96.4 (94.5-98.3) | NA | NA | NA | NA |
Abbreviations: ASC-H, atypical squamous cells cannot rule out HSIL; ASC-US, atypical squamous cells of undetermined significance; GBMSM, gay, bisexual, and other men who have sex with men; HRA, high-resolution anoscopy; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion; MMP, Medical Monitoring Project; NA, not applicable; PWH, persons with HIV; SCC, squamous cell carcinoma.
Data were collected during the 2019 MMP cycle and from a 2021 survey on HIV care facilities involving 2019 MMP participants.
Anal cytology results included negative, ASC-US, LSIL, HSIL, ASC-H, and SCC. The at least ASC-US category represents the sum of all results, excluding negative results. Categorization of PWH at highest risk was based on age, gender identity, sexual orientation, and anal cytology results.
Cytology results may not sum to the total for the respective risk group due to missing data in medical records abstraction.
The sum of at least ASC-US and negative cytology results totals 100%.
All PWH at highest risk included GBMSM or transgender women 35 years or older and all other PWH 45 years or older.
Coefficient of variation was 0.3 or greater. The estimate may be unstable and should be interpreted with caution.
The all other PWH 45 years or older group excluded GBMSM and transgender women 35 years or older.
Discussion
National guidelines recommend that anal cytology should not be performed without the ability to refer for HRA,4 but we found that a substantial number of PWH at highest risk of anal cancer may not have access to HRA on-site or by referral at their HIV care facility. With anal cancer prevention by diagnosis and treatment of cancer precursors now demonstrated,3 improvements in screening and early detection, including systematic monitoring of such efforts, are needed. Improvements may include expanded HRA training or certification, modified patient care workflow to encourage clinicians to perform or refer for screening, and increased education and awareness about symptoms among patients and clinicians. Anal cancer disproportionately affects subpopulations in regions with lower socioeconomic status.6 If screening or prevention improvements are not equitably implemented, they can increase rather than reduce disparities.
Study limitations include HRA availability data reported by facility staff, which might be subject to information bias. Additionally, some participants might have had cytology at facilities other than those we analyzed; however, less than 10% of participants reported receiving HIV care at more than 1 facility. Finally, cytology results among all PWH at highest risk may differ from those who were actually tested.
This study’s nationally representative estimates can inform large-scale implementation of anal cancer prevention efforts. Given the limited supply of clinicians who can perform HRAs and the number of potentially HRA-eligible persons, HRA capacity may be the rate-limiting factor in precancer treatment among PWH.
eAppendix. Ethical Consideration and Informed Consent of Study Participants
eMethods. Study Sample and Analysis
Data Sharing Statement
References
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
eAppendix. Ethical Consideration and Informed Consent of Study Participants
eMethods. Study Sample and Analysis
Data Sharing Statement
