Abstract
Objectives:
Women living with HIV (WLWH) have a greater risk of anal cancer than women without HIV, however there are limited studies that examine awareness of anal cancer risk among WLWH and “high-risk” HIV negative women. This study examines risk factors for anal cancer, perceptions of risk for anal cancer, and perceptions of anal cancer screening among a cohort of WLWH and high-risk HIV negative women.
Methods:
From the Atlanta, GA and Bronx, NY sites of the Women’s Interagency HIV Study (WIHS), 155 WLWH and HIV negative women were enrolled and the Champion Health Belief Model Scale questionnaire measuring risk perceptions to anal cancer was administered to each participant.
Results:
WLWH perceived anal cancer to be less serious and perceived facing fewer barriers to anal cancer screening than HIV negative women (both p=.01). Older women (>=50 years) felt they had less barriers to anal cancer screening (p=.047). Moreover, women who had less than a high school education felt more susceptible to anal cancer (p=.001), as did women who reported a history of anal intercourse (p=.017).
Conclusions:
Despite being at an increased risk for anal cancer, perceptions of susceptibility to anal cancer and seriousness of anal cancer were low among WLWH. These findings highlight opportunities for provider and patient educational interventions to improve awareness of anal cancer risk among WLWH.
Keywords: anal cancer, HIV, anal cytology, risk perceptions, cancer risk, health promotion, HPV knowledge, cancer prevention
Precis:
Despite being at an increased risk for anal cancer, perceptions of susceptibility and seriousness of anal cancer were low among women living with HIV.
INTRODUCTION
Although rare in the general population, anal cancers are more frequently detected in women than in men.1 Specifically, people living with HIV carry the burden for anal cancer cases, despite the advancement in antiretroviral therapy.2 For women living with HIV (WLWH) in the U.S., the annual incidence rate of anal cancer is 30/100,000 person years, compared to a rate of 1.9/100,000 in women of the general population.3,4 Furthermore, WLWH have up to five times greater risk of cervical cancer and 7.8 times greater risk of anal cancer than HIV negative women.5 Similar to cervical cancer, 90% of anal cancers worldwide are associated with high-risk human papillomavirus (HR-HPV).6 Frequently women, both HIV positive and negative have HPV infections, specifically types 16 and 18, concurrently in the cervix and anus.7,8 Moreover, studies show a higher prevalence of anal HPV positivity than cervical HPV positivity regardless of HIV status.9,10
Like the uterine cervix, the anal canal has a squamocolumnar junction that is susceptible to HR-HPV infection and HPV persistence that may lead to anal intraepithelial neoplasia (AIN) and invasive anal carcinoma.11 Anal cytology is a proposed initial tool to screen for anal neoplasia much like the current use of cervical cytology to screen for intraepithelial neoplasia.12 Over time, anal squamous intraepithelial lesions can either be cleared or slowly progress from low-grade squamous intraepithelial lesion (LSIL), to high-grade squamous intraepithelial lesions (HSIL), to anal intraepithelial neoplasia (AIN).13 Like cervical cytology screening, the goal of anal cytology screening is to detect and treat anal cancer precursors. However, the natural history of progression from normal anal epithelium to anal cancer associated with HR-HPV infection is not as well understood as that of the natural history of progression to cervical cancer. Hopefully, completion of a nationwide randomized clinical trial (Anal Cancer/HSIL Outcomes Research Study [ANCHOR], NCT 02135419) will provide more insight into that process as well as the effectiveness of treating anal neoplasia.
Currently, cervical cancer screening guidelines recommend enhanced screening for WLWH.14 However, no such formal guidance is provided for anal cancer screening among this cohort. Clinical experts familiar with identifying and managing anal neoplasia recommend use of anal cytology and high-resolution anoscopy (HRA) as being beneficial in the process of preventing occurrence of anal neoplasia and invasive cancer.15
Perceptions of health risk are important drivers of health behaviors. The Precaution Adoption Process Model acknowledges conscious awareness of a health risk is needed to adopt a new healthy behavior (i.e., screening) or cessation of a risky behavior.16 Moreover, risk awareness is the basis for receptivity to adopting behavior change that is linked to informed decision making. Despite the knowledge that WLWH are at increased risk of anal neoplasia and cancer the published literature pertaining to awareness of risk is sparse among both WLWH and high-risk HIV negative women. Furthermore, anal cancer shares similar risk factors with cervical cancer such as being immunocompromised, as with persons living with HIV, smoking, history of sexually transmitted infections (STI), more than three lifetime sexual partners, history of cervical intraepithelial neoplasia (CIN), and history of anal intraepithelial neoplasia (AIN).9,17–20 Thus, the purpose of this study is to explore risk factors, perceptions of anal cancer risk, and perceptions of anal cancer screening among a cohort of these women.
METHODS
Study Sample
A sample of women with and without HIV (n=155) were recruited and enrolled from the Atlanta, GA and Bronx, NY sites of the Women’s Interagency HIV Study (WIHS) from January 2015 to June 2015. The WIHS investigated the natural history of HIV disease in a cohort of HIV-positive women and a control cohort of high-risk HIV-negative women.21 The inclusion criteria for the WIHS are: 1) documented results for HIV-positive women or documented HIV-negative results within 30 days of enrollment for high-risk HIV-negative women; 2) no prior AIDS-related conditions; 3) documentation of laboratory reports of viral load and CD4+ counts for those on antiretroviral therapy; and 4) consent to store specimens in a national WIHS repository.21 For HIV negative women enrolled in the WIHS study, high-risk activity was defined as 1) injection drug use; 2) having a sexually transmitted disease; 3) engaging in unprotected sex with three or more men or protected sex with more than five men; or 4) past experience in exchanging sex for money or goods (i.e., drugs).21 Following the baseline visit, WIHS participants underwent a study-related visit every six months that comprises a sociodemographic questionnaire, blood, urine, and cervicovaginal specimen, and a physical and gynecologic exam. The eligibility criteria for our study included: 1) Enrolled in the WIHS study; 2) 25–60 years of age (recruitment age for WIHS V); 3) English speaking; and 4) willing to participate by completing two questionnaires assessing anal cancer and HPV knowledge and perceptions of anal cancer risk.
Study Protocol
Approvals from the Institutional Review Board at Emory University and research committees at the recruitment site were obtained. Three research assistants (RA) were trained to carry out recruitment through a standardized phone script for consent and administration of questionnaires. A list of eligible WIHS participants who met the inclusion criteria were contacted over the telephone by either the principal investigator (PI) or one of the trained RAs. Eligible women were asked to provide verbal informed consent to be enrolled in the study. Data collection was conducted over the phone where the PI or trained RA recorded the participants’ responses onto the paper questionnaires. At completion of the questionnaires, the participant was given a $25 gift card for participation and an informational handout with facts about cancer and HPV at their next WIHS study visit.
Questionnaires
Sociodemographic characteristics and risk factors such as HIV status, CD4+ count, history of anal intercourse, history of sexually transmitted infections, number of sexual partners, race, age, level of education and smoking status were obtained from the WIHS data repository (WIHS study visit #44).
The Champion Health Belief Model Scale (CHBMS) was administered to measure risk perceptions to anal cancer. This questionnaire was adapted to a 6th grade reading level and was previously tested in low income and African American women.22 Cronbach’s alpha was 0.84, which suggests high internal scale reliability and is consistent with prior reports.22 The CHBMS is a 41-item Likert scale questionnaire with five subscales that were adapted to measure perceptions of anal cancer and anal cancer screening. The five subscales are perceived susceptibility to anal cancer, perceived seriousness of anal cancer, perceived benefits and barriers to anal cytology testing, and general health motivation with 5-point Likert scale responses ranging from “strongly agree” (5) to “strongly disagree” (1) to each health belief statement. The overall score range for the susceptibility subscale is 6–30, the seriousness subscale is 12–60, perceived benefits subscale is 5–25, and perceived barriers subscale 8–40 (the general health motivation subscale is not reported). The responses result in a summative score for each subscale where a higher score is indicative of higher levels of that perception.
Data management and Statistical Analysis
SPSS version 27 software (Armonk, NY: IBM Corp.) was employed for data entry and descriptive statistical analysis of health beliefs related to anal cancer and HPV. Data were entered directly into SPSS and double entry was used to minimize errors. Data discrepancies were detected by the SPSS Compare Datasets command. All discrepancies were compared to the original response and corrected by the PI. A summed score was obtained for each of the five subscales (general health motivation subscale is not reported) and means compared by HIV status (+ or -). Correlations were explored using analysis of variance (ANOVA) between risk perception scores and sociodemographic and risk factors. Differences between groups by HIV status or risk factors were explored using Student’s t-test or Chi-square tests with a significance level of 0.05, unless specified otherwise.
Role of funding sources
The funding source had no role in study design, data collection, data analysis, or interpretation of findings.
RESULTS
Sample Characteristics
Table 1 describes the characteristics of the study sample. Of the 155 women enrolled from the Atlanta and Bronx WIHS sites, 65.8% of the sample (n=102) were HIV positive and 34.2% (n=53) were high risk HIV negative. The mean age was 47 years (SD= 9.46) and did not differ by status. A majority of the participants were Black/non-Hispanic (85.7%), with smaller numbers of white non-Hispanic (5.2%) and other (5.9%). Sixty four percent of the sample reported completing high school or higher. Almost half (49%) of the sample are current smokers and report a history of an abnormal cervical cytology. About 41% reported history of gonorrhea, 46% history of chlamydia, 19% history of herpes, 24% history of syphilis, and 16% history of genital warts. More WLWH reported a diagnoses of STIs and these were significant for gonorrhea and herpes. The mean for lifetime male sexual partners was 90.6 (SD= 317.7).
Table 1:
Sample demographics and clinical characteristics by HIV status
| Characteristic | Overall N (%) |
HIV Positive (n=102)a |
HIV Negative (n= 53)b |
P-valuec |
|---|---|---|---|---|
|
| ||||
| Mean age (range) | 46.95 (26–68) | 48.07 (26–68) | 44.78 (26–67) | .059d |
| Mean CD4+ count | 594.24 | N/A | -- | |
| Race/Ethnicity | ||||
| White (non-Hispanic) | 8 (5.2) | 3 (3) | 5 (9.4) | .239 |
| White (Hispanic) | 2 (1.3) | 2 (2) | 0 (0) | |
| Black (non-Hispanic) | 132 (85.7) | 88 (87.1) | 44 (83) | |
| Black (Hispanic) | 3 (1.9) | 2 (2) | 1 (1.9) | |
| Other | 9 (5.9) | 7 (5.9) | 2 (5.7) | |
| Education | ||||
| Grade school or les | 2 (1.3) | 2 (2) | 0 (0) | .336 |
| Grades 7–11 | 53 (34.4) | 38 (37.3) | 15 (28.3) | |
| High school | 37 (24) | 22 (21.6) | 15 (28.3) | |
| Some college | 51 (33.1) | 34 (33.3) | 17 (32.1) | |
| Completed college | 7 (4.5) | 4 (3.9) | 3 (5.7) | |
| Attended/completed graduate school | 4 (2.6) | 1 (1) | 3 (5.7) | |
| Smoking Status | ||||
| Current Smoker | 76 (49.4) | 48 (48.1) | 28 (52.8) | .612 |
| Never smoked/ former smoker | 78 (50.6) | 53 (51.9) | 25 (47.2) | |
| Ever had cervical cytology? | ||||
| Yes | 144 (92.9) | 95(93.1) | 49 (92.5) | .715 |
| No | 1 (.6) | 1 (1) | 0 (0) | |
| Don’t know/skipped | 10 (26) | 6 (5.9) | 4 (7.5) | |
| Ever had abnormal cervical cytology? | ||||
| Yes | 76 (49) | 52 (51) | 24 (45.3) | .782 |
| No | 75 (48.4) | 47 (46.1) | 28 (52.8) | |
| Don’t know/skipped | 4 (2.6) | 3 (2.9) | 1 (1.9) | |
| Ever been told had gonorrhea? | ||||
| Yes | 63 (40.6) | 48 (47.1) | 15 (28.3) | .036 |
| No | 90 (58) | 52 (51) | 38 (71.7) | |
| Don’t know/ skipped | 2 (1.4) | 2 (2) | 0 (0) | |
| Ever been told had chlamydia? | .175 | |||
| Yes | 71 (45.8) | 51 (50) | 20 (37.7) | |
| No | 84 (54.2) | 51 (50) | 33 (62.3) | |
| Don’t know/ skipped | 0 (0) | 0 (0) | 0 (0) | |
| Ever been told had herpes? | .004 | |||
| Yes | 30 (19.4) | 27 (26.5) | 3 (5.7) | |
| No | 124 (80) | 75 (73.5) | 49 (92.5) | |
| Don’t know/ skipped | 1 (.6) | 0 (0) | 1 (1.9) | |
| Ever been told had syphilis? | .094 | |||
| Yes | 37 (23.9) | 29 (28.4) | 8 (15.1) | |
| No | 116 (74.8) | 71 (69.6) | 45 (84.9) | |
| Don’t know/ skipped | 2 (1.3) | 2 (2) | 0 (0) | |
| Ever been told had genital warts? | .357 | |||
| Yes | 25 (16.1) | 19 (18.6) | 6 (11.3) | |
| No | 130 (83.9) | 83 (81.4) | 47 (88.7) | |
| Don’t know/ skipped | 0 (0) | 0 (0) | 0 (0) | |
| Mean lifetime sexual partners (SD) | ||||
| Male sexual partners | 90.6 (317.7) | 88.2 (326.9) | 95.1 (302.5) | .885d |
| Female sexual partners | 11.7 (61.8) | 16.2 (77.8) | 3.8 (2.5) | .491d |
| History of anal intercourse with men | ||||
| Yes | 65 (41.9) | 46 (45.1) | 19 (35.8) | .306 |
| No | 90 (58.1) | 56 (54.9) | 34 (64.2) | |
missing= 1
missing=2
Chi-square test unless specified
Independent samples t-test
Perceptions of Anal Cancer and Anal Cancer Screening
Mean scores and correlates for the four subscales are depicted in Table 2. The mean perceived susceptibility score for anal cancer was 13.44 (SD= 4.64); mean score for perceived seriousness of anal cancer was 32.78 (SD= 9.33); mean score for perceived benefits of anal cancer screening was 20.10 (SD= 2.63); mean score for perceived barriers to anal cancer screening was 18.54 (SD= 4.52).
Table 2.
Correlates of sociodemographic, risk factors and perceptions of risk.
| Sample characteristic | Susceptibility to anal cancer (range 6–30) Mean (SD) | Seriousness of anal cancer (range 12–60) Mean (SD) | Benefits of anal cancer screening (range 5–25) Mean (SD) | Barriers to anal cancer screening (range 8–40) Mean (SD) | |
|---|---|---|---|---|---|
| HIV status | negative | 12.77 (4.35) | 35.28 (8.92)* | 20.02 (2.71) | 19.75 (4.98)* |
| positive | 13.85 (4.78) | 31.45 (9.39) | 20.18 (2.61) | 17.92 (4.20) | |
| Age | < 50 years | 13.55 (4.30) | 33.14 (8.77) | 20.00 (2.66) | 19.20 (4.48)* |
| ≥ 50 years | 13.32 (5.03) | 32.35 (9.99) | 20.21(2.61) | 17.76 (4.48) | |
| Race | White, non-Hispanic | 11.57 (4.58) | 32.25 (4.77) | 18.38 (2.45) | 19.50 (6.76) |
| Black, non-Hispanic | 13.44 (4.71) | 32.93 (9.95) | 20.19 (2.67) | 18.45 (4.53) | |
| Hispanic | 15.30 (3.56) | 30.90 (4.77) | 20.70 (2.16) | 18.30 (3.89) | |
| other | 11.25 (1.50) | 30.50 (5.20) | 19.00 (1.15) | 20.00 (2.31) | |
| Education | High school or less | 14.41 (4.96)* | 33.91 (8.71) | 20.11 (2.93) | 18.55 (3.90) |
| some college or more | 11.98 (3.63) | 30.90 (10.11) | 20.08 (2.13) | 18.50 (5.43) | |
| Current cigarette smoking status | Not currently smoking | 12.87 (5.19) | 31.47 (9.75) | 20.14 (2.77) | 18.32 (4.80) |
| Currently Smoking | 13.97 (3.89) | 33.96 (8.88) | 20.05 (2.49) | 18.75 (4.32) | |
| Abnormal cervical cytology | Yes | 13.87 (4.59) | 32.76 (9.75) | 20.22 (2.59) | 18.61 (4.55) |
| No | 13.18 (4.78) | 32.53 (9.12) | 19.97 (2.75) | 18.37 (4.59) | |
| Ever told gonorrhea | Yes | 13.24 (4.63) | 30.57 (8.73)* | 20.51 (2.56) | 17.84 (4.48) |
| No | 13.55 (4.54) | 34.10 (9.58) | 19.89 (2.68) | 19.04 (4.61) | |
| Ever told syphilis | Yes | 13.64 (4.65) | 31.22 (8.79) | 19.78 (2.27) | 18.19 (4.01) |
| No | 13.36 (4.56) | 33.13 (9.55) | 20.23 (2.76) | 18.57 (4.66) | |
| Ever told chlamydia | Yes | 13.34 (4.70) | 32.42 (9.64) | 20.31 (2.71) | 18.15 (4.55) |
| No | 13.60 (4.64) | 33.05 (9.21) | 19.96 (2.58) | 18.88 (4.55) | |
| Ever told herpes | Yes | 14.93 (4.98) | 32.03 (8.78) | 21.03 (2.75)* | 17.37 (3.85) |
| No | 13.15 (4.55) | 32.86 (9.55) | 19.92 (2.58) | 18.77 (4.63) | |
| Ever told warts in or around genital area | Yes | 14.88 (3.58) | 32.00 (8.03) | 19.92 (2.53) | 18.24 (4.55) |
| No | 13.22 (4.80) | 32.91 (9.64) | 20.16 (2.66) | 18.61 (4.57) | |
| # lifetime male partners >20 | No | 13.52 (4.90) | 33.46 (8.80) | 20.27 (2.47) | 18.80 (4.20) |
| Yes | 13.39 (4.36) | 31.63 (10.07) | 19.92 (2.88) | 18.18 (5.03) | |
| Ever had anal intercourse with men | No | 12.72 (4.52)* | 32.27 (9.59) | 20.10 (2.67) | 18.33 (4.86) |
| Yes | 14.55 (4.68) | 33.45 (9.11) | 20.15 (2.61) | 18.85 (4.10) |
Note:
Indicates the group means of the domain scores are significantly different (P <0.05)
WLWH women perceived anal cancer to be less serious (mean scores= 31.45 [SD= 9.39] versus 35.28 [SD= 8.92]) and additionally perceived facing fewer barriers to anal cancer screening than HIV negative women (mean scores= 17.92 [SD=4.20] versus 19.75 [SD= 4.98], respectively; both p=.01). Older women (>=50 years) reported fewer barriers to anal cancer screening (mean scores= 17.76 [SD= 4.48] versus 19.20 [SD= 4.48]; p=.047). Moreover, women who had less than a high school diploma perceived to have an increase susceptibility to anal cancer (mean scores= 14.41 [SD= 4.96] versus 11.98 [SD= 3.63]; p=.001). Women who reported a history of anal intercourse felt more susceptible to anal cancer (mean scores= 14.55 [SD= 4.68] versus 12.72 [SD= 4.52]; p=.017). Women with a history of gonorrhea felt anal cancer was less serious of a disease than those without a history of gonorrhea (mean scores= 30.57 [SD= 8.73] versus 34.10 [SD= 9.58]; p= .020). However, women with a history of herpes found anal cytology to be more beneficial at detecting anal cancer than their herpes negative counterparts (mean scores= 21.03 [SD= 2.75] versus 19.92 [SD= 2.58]; p= .050).
DISCUSSION
Perceptions of the benefit of anal cancer screening were high among this sample and did not differ by HIV status, yet barriers to anal cancer screening were perceived to be high and significantly differed by HIV status. WLWH had a lower perception of barriers to anal cancer screening than women without HIV perhaps due to having increased interactions with infectious disease clinicians, and more opportunities for heightened surveillance and screening efforts. Additionally, WLWH may have more access to anal cytology testing and associated screening efforts if managed at a comprehensive HIV care clinic, as the women in this study. Although our study did not measure adherence to anal cancer screening, other studies have shown a relationship between perceived barriers to cervical cytology testing and adherence to cervical cancer screening among HIV positive and HIV negative women.23–26 These studies show the importance of increasing access to cancer screening in order to have a successful cancer prevention plan among high risk populations.
Women in this study reported several risk factors known to be associated with greater risk of anal neoplasia and cancer.9,10,17–19 Despite having these risk factors, WLWH in our study viewed anal cancer to be less serious than HIV negative women. Similarly in the cervical cancer literature, perceptions of seriousness and susceptibility to cervical cancer were found to be low in WLWH.27 Whereas, another study found an increased perception of susceptibility led to increase cervical cancer screening uptake.28 These findings highlight the importance of education about anal cancer, particularly for populations at high risk, to increase the perceptions of risk to potentially increase anal cancer screening uptake.
Although our study sheds light on the perceptions of anal cancer risk among a high risk group of women, we acknowledge limitations to this study. First, risk factors were extracted from the WIHS repository of self-reported questionnaires thus we were limited in accessing other risk factors such as history of HPV. Furthermore, due to the sensitive nature of questions on sexual behaviors and activities, some women may have reported an inaccurate representation of actual risk factors regarding sexual behavior. Second, this study was conducted in a sample of women who were enrolled in a large longitudinal study that required research visits every six months. Thus, increased encounters and involvement with research clinicians allow for greater accessibility to resources and patient education, which may not be representative of women of the general population. Women of the general population may lack a similar opportunity to obtain individual risk information that may shape perceptions and influence health behaviors. Lastly, non-English speaking participants were excluded from this study, which limits generalizability to non-English speaking populations.
CONCLUSION
Our findings highlight opportunities for provider and patient educational interventions to improve awareness of anal cancer risk among WLWH and HIV negative women at risk for HPV. Furthermore, with an aging HIV population, it is an essential public health goal to provide the necessary resources and cancer prevention strategies for persons living with HIV to achieve a normal life expectancy and quality of life. Understanding perceptions of risk for anal cancer in a sample of high risk women is essential to develop interventions to promote informed decision making about preventive action and enhances participation in recommended screening.
Funding source:
This study was funded by a supplement award to the Women’s Interagency HIV Study (U01-AI103408-SUPPLEMENT). Data in this manuscript were collected by the Women’s Interagency HIV Study, now the MACS/WIHS Combined Cohort Study (MWCCS).
The contents of this publication are solely the responsibility of the authors and do not represent the official views of the National Institutes of Health (NIH). MWCCS (Principal Investigators): Atlanta CRS (Ighovwerha Ofotokun, Anandi Sheth, and Gina Wingood), U01‐HL146241; Baltimore CRS (Todd Brown and Joseph Margolick), U01‐HL146201; Bronx CRS (Kathryn Anastos and Anjali Sharma), U01 HL146204; Brooklyn CRS (Deborah Gustafson and Tracey Wilson), U01‐HL146202; Data Analysis and Coordination Center (Gypsyamber D’Souza, Stephen Gange and Elizabeth Golub), U01‐HL146193; Chicago‐Cook County CRS (Mardge Cohen and Audrey French), U01‐HL146245; Chicago‐Northwestern CRS (Steven Wolinsky), U01‐ HL146240; Connie Wofsy Women’s HIV Study, Northern California CRS (Bradley Aouizerat and Phyllis Tien), U01‐HL146242; Los Angeles CRS (Roger Detels), U01‐HL146333; Metropolitan Washington CRS (Seble Kassaye and Daniel Merenstein), U01‐HL146205; Miami CRS (Maria Alcaide, Margaret Fischl, and Deborah Jones), U01‐HL146203; Pittsburgh CRS (Jeremy Martinson and Charles Rinaldo), U01‐HL146208; UAB‐MS CRS (Mirjam‐Colette Kempf and Deborah Konkle‐Parker), U01‐HL146192; UNC CRS (Adaora Adimora), U01‐HL146194. The MWCCS is funded primarily by the National Heart, Lung, and Blood Institute (NHLBI), with additional co‐funding from the Eunice Kennedy Shriver National Institute Of Child Health & Human Development (NICHD), National Human Genome Research Institute (NHGRI), National Institute On Aging (NIA), National Institute Of Dental & Craniofacial Research (NIDCR), National Institute Of Allergy And Infectious Diseases (NIAID), National Institute Of Neurological Disorders And Stroke (NINDS), National Institute Of Mental Health (NIMH), National Institute On Drug Abuse (NIDA), National Institute Of Nursing Research (NINR), National Cancer Institute (NCI), National Institute on Alcohol Abuse and Alcoholism (NIAAA), National Institute on Deafness and Other Communication Disorders (NIDCD), National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK). MWCCS data collection is also supported by UL1‐ TR000004 (UCSF CTSA), P30‐AI‐050409 (Atlanta CFAR), P30‐AI‐050410 (UNC CFAR), and P30‐AI‐027767 (UAB CFAR).
List of Abbreviations and Acronyms
- HIV
Human Immunodeficiency Virus
- HPV
Human Papillomavirus
- HR-HPV
High Risk Human Papillomavirus
- WLWH
women living with HIV
- STI
sexually transmitted infection
- CIN
cervical intraepithelial neoplasia
- WIHS
women interagency HIV study
Footnotes
Declaration of Interests
All authors declare no conflicts of interest.
IRB status: This study was approved by Emory University’s Institutional Review Board (00077173) and by Grady Healthcare System Research Oversight Committee.
REFERENCES
- 1.Silverberg MJ, Lau B, Justice AC, et al. Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clinical Infectious Diseases. 2012;54(7):1026–1034. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Crum-Cianflone NF, Hullsiek KH, Marconi VC, et al. Anal cancers among HIV-infected persons: HAART is not slowing rising incidence. AIDS (London, England). 2010;24(4):535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Shiels MS, Pfeiffer RM, Chaturvedi AK, Kreimer AR, Engels EA. Impact of the HIV epidemic on the incidence rates of anal cancer in the United States. J Natl Cancer Inst. 2012;104(20):1591–1598. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Deshmukh AA, Suk R, Shiels MS, et al. Incidence trends and burden of human papillomavirus-associated cancers among women in the United States, 2001–2017. JNCI: Journal of the National Cancer Institute. 2021;113(6):792–796. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Denslow SA, Rositch AF, Firnhaber C, Ting J, Smith JS. Incidence and progression of cervical lesions in women with HIV: A systematic global review. Int J STD AIDS. 2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.de Martel C, Plummer M, Vignat J, Franceschi S. Worldwide burden of cancer attributable to HPV by site, country and HPV type. International journal of cancer. 2017;141(4):664–670. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Lin C, Slama J, Gonzalez P, et al. Cervical determinants of anal HPV infection and high-grade anal lesions in women: a collaborative pooled analysis. The Lancet Infectious Diseases. 2019;19(8):880–891. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Veo CA, Saad SS, Fregnani JHT, et al. Clinical characteristics of women diagnosed with carcinoma who tested positive for cervical and anal high-risk human papillomavirus DNA and E6 RNA. Tumor Biology. 2015;36(7):5399–5405. [DOI] [PubMed] [Google Scholar]
- 9.Hidalgo-Tenorio C, de Jesus SE, Esquivias J, Pasquau J. High prevalence and incidence of HPV-related anal cancer precursor lesions in HIV-positive women in the late HAART era. Enfermedades infecciosas y microbiologia clinica (English ed). 2018;36(9):555–562. [DOI] [PubMed] [Google Scholar]
- 10.Slama J, Sehnal B, Dusek L, Zima T, Cibula D. Impact of risk factors on prevalence of anal HPV infection in women with simultaneous cervical lesion. Neoplasma. 2015;62(2):308–314. [DOI] [PubMed] [Google Scholar]
- 11.Darragh TM, Winkler B. Anal cancer and cervical cancer screening: key differences. Cancer Cytopathol. 2011;119(1):5–19. [DOI] [PubMed] [Google Scholar]
- 12.Wells JS, Holstad MM, Thomas T, Bruner DW. An integrative review of guidelines for anal cancer screening in HIV-infected persons. AIDS Patient Care STDS. 2014;28(7):350–357. [DOI] [PubMed] [Google Scholar]
- 13.Machalek DA, Poynten M, Jin F, 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(5):487–500. [DOI] [PubMed] [Google Scholar]
- 14.Robbins HA, Strickler HD, Massad LS, et al. Cervical cancer screening intervals and management for women living with HIV: a risk benchmarking approach. AIDS. 2017;31(7):1035–1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Palefsky JM. Anal cancer prevention in HIV-positive men and women. Curr Opin Oncol. 2009;21(5):433. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Weinstein ND, Sandman PM, Blalock SJ. The precaution adoption process model. The Wiley Encyclopedia of Health Psychology. 2020:495–506. [Google Scholar]
- 17.Daling JR, Madeleine MM, Johnson LG, et al. Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer. Cancer. 2004;101(2):270–280. [DOI] [PubMed] [Google Scholar]
- 18.Holly EA, Ralston ML, Darragh TM, Greenblatt RM, Jay N, Palefsky JM. Prevalence and risk factors for anal squamous intraepithelial lesions in women. J Natl Cancer Inst. 2001;93(11):843–849. [DOI] [PubMed] [Google Scholar]
- 19.Palefsky JM, Holly EA, Ralston ML, Da Costa M, Greenblatt RM. Prevalence and risk factors for anal human Papillomavirus infection in Human Immunodeficiency Virus (HIV)-positive and high-risk HIV-negative women. J Infect Dis. 2001;183(3):383–391. [DOI] [PubMed] [Google Scholar]
- 20.Palefsky JM, Holly EA, Ralston ML, Jay N. Prevalence and risk factors for human papillomavirus infection of the anal canal in human immunodeficiency virus (HIV)-positive and HIV-negative homosexual men. J Infect Dis. 1998;177(2):361–367. [DOI] [PubMed] [Google Scholar]
- 21.Bacon MC, von Wyl V, Alden C, et al. The Women’s Interagency HIV Study: an observational cohort brings clinical sciences to the bench. Clin Diagn Lab Immunol. 2005;12(9):1013–1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Massad LS, Evans CT, Weber KM, et al. Changes in knowledge of cervical cancer prevention and human papillomavirus among women with human immunodeficiency virus. Obstet Gynecol. 2010;116(4):941–947. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Bukirwa A, Mutyoba JN, Mukasa BN, et al. Motivations and barriers to cervical cancer screening among HIV infected women in HIV care: a qualitative study. BMC Womens Health. 2015;15(1):1–11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Fletcher FE, Buchberg M, Schover LR, et al. Perceptions of barriers and facilitators to cervical cancer screening among low-income, HIV-infected women from an integrated HIV clinic. AIDS Care. 2014;26(10):1229–1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Marlow LA, Waller J, Wardle J. Barriers to cervical cancer screening among ethnic minority women: a qualitative study. J Fam Plann Reprod Health Care. 2015;41(4):248–254. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Lambert CC, Chandler R, McMillan S, Kromrey J, Johnson-Mallard V, Kurtyka D. Pap Test Adherence, Cervical Cancer Perceptions, and HPV Knowledge Among HIV-Infected Women in a Community Health Setting. J Assoc Nurses AIDS Care. 2015;26(3):271–280. [DOI] [PubMed] [Google Scholar]
- 27.Lambert C, Crystal L. Factors Influencing Cervical Cancer Screening in Women Infected With HIV: A Review of the Literature. J Assoc Nurses AIDS Care. 2012. [DOI] [PubMed] [Google Scholar]
- 28.Wong Y-L, Chinna K, Mariapun J, Shuib R. Correlates between risk perceptions of cervical cancer and screening practice. Prev Med. 2013;57:S24–S26. [DOI] [PubMed] [Google Scholar]