Abstract
Background:
The incidence of anal cancer in HIV positive women is a growing public health concern where they have a 7.8 fold increased risk for anal cancer than women in the general population. We examined knowledge of anal cancer, anal cancer screening and HPV in HIV positive women and high-risk HIV negative women.
Methods:
Women were recruited from the Women’s Interagency HIV Study and completed an adapted Knowledge of Anal Cancer and HPV Scale. Correlations among anal cancer knowledge and sociodemographic and risk factors were assessed using Pearson’s or Spearman Rho r test. Student’s t test or Chi –square tests identified significant differences between groups by HIV-status or risk factors.
Results:
Among 155 women, 72% (n=113) correctly identified the purpose of an anal Pap test. However, only 42% (n=65) identified HIV as a risk factor for anal cancer. HIV positive women were more knowledgeable about anal cancer than HIV negative women (t=2.104, p=.037). Women with a history of an abnormal cervical Pap test (t=2.137, p=.034), younger age (t= 3.716, p= .000), reported history of anal sex (t= 3.284, p= .001), some college education or higher (t= −2.005, p=.047), and non-smokers (t=2.425, p=.016) were significantly more knowledgeable about HPV.
Conclusions:
Although most women were knowledgeable about anal cancer, many women could not identify important risk factors for anal cancer, such as HIV infection. Patient educational interventions tailored to HIV positive women are warranted to improve knowledge and awareness of risk for anal cancer.
INTRODUCTION
Although anal cancer is rare in the general population, the incidence among HIV positive individuals is alarmingly high. From 1996-2007, the incidence of anal cancer in HIV positive women was 30 per 100,000 person-years; whereas, no anal cancer cases were observed in HIV negative women during the same time frame [1]. Furthermore, HIV positive women have a 7.8 fold increased risk for anal carcinoma in situ compared to women in the general population [2].
Similar to its well-known relationship with cervical cancer, HPV infection is a significant cause of anal intraepithelial lesions and 80% of anal cancer cases in the US [3]. In fact, anal HPV infection is found to be more common than cervical HPV in both HIV positive and HIV negative U.S. women [4, 5]. Immunosuppression plays a significant role in the high prevalence and persistence of HPV infections seen in HIV positive individuals. Individuals living with HIV have an increased risk for acquiring a HPV infection and are more likely to have persistent HPV induced anal dysplasia, thus increasing their risk for anal cancer [6].
Similar to the cervix, the anal canal has a transformation zone that is vulnerable to dysplasia from HPV infection [7]. Analogous to cervical cancer screening, there is a similar approach to anal cancer screening using an anal Papanicolaou (Pap) test as a screening procedure to detect pre-cancerous changes in the anal canal. However, unlike cervical cancer screening, no standardized or formal guidelines exist for anal cancer screening for HIV positive individuals due to the lack of randomized control trials to test the reliability and validity of a screening program for anal cancer. However, informal guidelines and recommendations from authoritative agencies and expert opinions recommend the use of anal cancer screening in HIV positive individuals with anal cytology or, at a minimum, digital rectal examination [8, 9]. The New York State Department of Public Health AIDS Institute recommends a digital rectal examination along with targeted annual anal Pap tests for MSMs, all HIV positive patients with a history of anogenital warts, and HIV positive women with a history of cervical or vulvar dysplasia [10]. Albeit the lack of supportive evidence, anal cancer screening integrated as part of a comprehensive management plan for HIV positive individuals is suggested to be the best approach in efforts to alter the increasing clinical burden of anal cancer in HIV positive individuals [10, 11].
Knowledge of the risk of cervical cancer associated with HPV has been well studied, both in the general population, and among HIV positive women. Low risk perception and lack of knowledge have been associated with low cervical cancer screening rates in the general population [12]. Substantial knowledge deficits exist regarding cervical cancer prevention and HPV among HIV positive women; in one study, 53% of the women incorrectly believed that cervical cancer was not preventable,[13] and 50% of HIV positive women in another study knew that HPV caused cervical cancer [14].
There is a paucity of data examining knowledge of HPV and its association with anal cancer among the general population, as well as among those most at risk, such as HIV positive individuals. A study with men who have sex with men found that the men in the study knew very little about anal cancer and HPV. Fifty-five percent had never heard of an anal Pap smear and 44.8% had never heard of HPV and whether the virus affected men or women [15]. Although HIV positive women have an increased risk for anal cancer, there is very limited data that explores knowledge and perceptions of their risk for anal cancer.
We examined knowledge of anal cancer screening, risk factors for anal cancer and its association with HPV using the AIDS Risk Reduction Model framework, a three stage model originally used to understand the psychosocial determinants of safer sexual practices and harm reduction in individuals at risk for HIV [16]. According to the model, knowledge is a prerequisite to recognize risk and to take action to change or reduce the risk. Risk factors for anal HPV infection in HIV positive women include low CD4+ count (<200 cells/mm3), cervical HPV infection or cytology, and younger age [4]. Risk factors for anal dysplasia and/or cancer in HIV positive women are anoreceptive intercourse, current smoker, >15 lifetime sexual partners, younger age, presence of anal HPV, history or concurrent abnormal cervical cytology, low CD4+ count, increase HIV viral load, and history of sexually transmitted infections (gonorrhea and genital warts) [17-20]. Increases in the prevalence of these exposures may account for the increasing incidence of anal cancer in HIV positive women. We focused on Stage 1 of the model to understand anal cancer and HPV knowledge and perceived risks in a sample of HIV positive women and a comparison group of high-risk HIV negative women.
MATERIALS AND METHODS
Study Population
We recruited 155 HIV positive and high-risk negative women from the Atlanta, GA and Bronx, NY sites of the Women’s Interagency HIV Study (WIHS) from January 2015- June 2015. WIHS is a large, ongoing, comprehensive, prospective cohort study of the natural history of HIV disease in a cohort of HIV positive women and a comparison cohort of high-risk HIV negative women [21]. Enrollment for WIHS began in 1993 with currently nine subsites throughout the United States. The Bronx site is part of the initial enrollment phase; the Atlanta, GA subsite was added in 2013. The WIHS inclusion criteria are: 1) documented HIV positive or for high-risk HIV negative women, documented HIV negative results within 30 days of enrollment; 2) no history of AIDS-related conditions; 3) documentation of laboratory reports of viral load and CD4+ counts for those who are on antiretroviral therapy; 4) consent to store specimens in a national WIHS repository. High-risk HIV negative women are defined as 1) injection drug use; 2) having a sexually transmitted disease; 3) unprotected sex with three or more men or protected sex with five or more men; or 4) history of exchange sex for money or goods. Women enrolled in the WIHS study have a study related visit every six months after the baseline visit. The interview includes a battery of sociodemographic questionnaires, blood, urine, and cervicovaginal specimen for laboratory parameters, and a physical and gynecologic exam [22, 21]. The inclusion criteria for participation in the current sub-study were: 1) enrolled in the parent WIHS study; 2) English speaking; 3) willing to participate by completing two questionnaires over the phone that assess anal cancer and HPV knowledge and perceptions of anal cancer risk.
Study Procedures
Approval from the Institutional Review Board of Emory University and research committees at the recruitment site were granted before commencement of enrollment. The Principal Investigator (PI) trained three research assistants to use a standardized phone script for consent and administration of the questionnaires. A list of WIHS participants’ contact information was generated and then each WIHS participant was contacted over the telephone by either the PI or one of three trained research assistants. Once contacted, the purpose of the sub-study was described, what participation entails, and the inclusion criteria. Potential participants who met the inclusion criteria and provided verbal informed consent were enrolled in the study. Study participants completed two interviewer-administered questionnaires over the phone. The trained RA or PI read each question to the participant over the phone and recorded the participant’s responses onto the paper questionnaire. After completion of the questionnaires, the participant received a $25 gift card for participation at her next WIHS study visit.
Questionnaires
The Knowledge of Anal Cancer and HPV scale was adapted to a 6th grade reading level and was previously tested in low income and African American women [13, 23]. Cronbach alpha for this study was 0.76, which is consistent with prior reports [23].
Knowledge of Anal Cancer and HPV is a 44-item knowledge multiple choice survey adapted from the Hild-Mosely et al study [24]. The original questionnaire measures knowledge about HPV, cervical Pap tests, risk factors, and HPV vaccination. For this study, “cervical” was substituted with “anal” along with other minor modifications for ease of understanding. To help decrease guessing, “I don’t know” was added as an answer choice. A percentage score of correct responses was calculated and range from 0 to 100.
Sociodemographic characteristics and risk factors of age, race, level of education, CD4+ count, HIV status, history of cervical cytology, history of anal intercourse, smoking status, number of lifetime sexual partners, and history of sexually transmitted infections were obtained from the parent WIHS follow up visit data for each participant. After study completion, participants were offered a handout of information and facts about anal cancer and HPV at their next WIHS study visit.
Data management and analysis
Data was entered directly into a SPSS version 23 database. Double entry was used to minimize errors and the SPSS Compare Datasets command was employed to detect data discrepancies. Discrepancies were then compared to the original questionnaire and corrected by the PI. Descriptive statistical analysis of the level of knowledge related to anal cancer and HPV was performed using SPSS version 23 software. For analysis of the Knowledge scale, frequencies of correct responses were calculated where an 1 was assigned for each correct response and 0 was assigned for each incorrect or “don’t know” response. Correct responses to questions pertaining to anal cancer and anal pap testing were summed and divided by the number of questions in the section and multiplied by 100 to create a percentage score. Similarly, a percentage score was created for questions related to HPV knowledge. Correlations were explored using Pearson’s or Spearman Rho r test between knowledge and health belief scores and sociodemographic and risk factors. Student’s t test or Chi –square tests identified significant differences between groups by HIV-status or risk factors. Unless mentioned otherwise, statistical testing used two-sided tests and a significance level of 0.05.
RESULTS
Of the 155 women enrolled, 83 % (n=131) were enrolled from the Atlanta site and 17% (n=26) from the Bronx site. Mean age was 47 years, 86% of participants are non-Hispanic black, 65% are HIV positive, and 49% are current smokers (Table 1). About one third of the women reported completing education between grades 7-11, and an addition third reported some college. Median lifetime male partners reported was 20 (range, 1-3000) and median lifetime female partners was three (range, 1-500). Among HIV positive women, mean CD4+ lymphocyte cell counts were 594 cells/mm3.
Table 1:
Study Characteristics
| Sociodemographic Variable |
Overall N (%) |
HIV Positive (n=102) |
High-risk HIV Negative (n= 53) |
P-valuea |
|---|---|---|---|---|
| Mean age (range) | 46.95 (26-68) | 48.07 (26-68) | 44.78 (26-67) | .059b |
| WIHS site | ||||
| Atlanta, GA | 129 (83.2%) | 81 (52.3%) | 48 (31%) | .112 |
| Bronx, NY | 26 (16.8%) | 5 (3.2%) | 21 (13.5%) | |
| 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 | ||||
| No schooling | 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 | 4 (2.6) | 1 (1) | 3 (5.7) | |
| graduate school | ||||
| Smoking Status | ||||
| Current Smoker | 76 (49.4) | 48 (48.1) | 28 (52.8) | .612 |
| Never smoked/ former | 78 (50.6) | 53 (51.9) | 25 (47.2) | |
| smoker | ||||
| Ever had a cervical Pap test? | ||||
| Yes | 144 (92.9) | 95 (93.1) | 49 (92.4) | .662 |
| No | 1 (.6) | 1 (.9) | 0 (0) | |
| Don’t know/skipped | 10 (6.5) | 6 (6) | 4 (7.6) | |
| Ever had an abnormal cervical Pap test? | ||||
| 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? | 1.75 | |||
| 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? | ||||
| Yes | 30 (19.4) | 27 (26.5) | 3 (5.7) | .004 |
| 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? | ||||
| Yes | 37 (23.9) | 29 (28.4) | 8 (15.1) | .094 |
| 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? | ||||
| Yes | 25 (16.1) | 19 (18.6) | 6 (11.3) | .357 |
| No | 130 (83.9) | 83 (81.9) | 47 (88.7) | |
| Don’t know/ skipped | 0 (0) | 0 (0) | 0 (0) | |
| Mean lifetime partners (range; median) | ||||
| Male | 90.58 (1-3000; 317.7) | 88.2 (1-3000; 20.0) | 95.0 (3-2000; 20.0) | .885b |
| Female | 11.67 (1-500; 67.84) | 16.24 (1-500; 2.0) | 3.8 (1-10; 3.5) | .491b |
Chi-square test unless specified
Independent samples t-test
Knowledge about Anal Cancer and Anal Pap Tests
The average score of correct responses for Anal Cancer Knowledge for the overall sample was 56%; by status, the average score was 57% for HIV positive women and an average score of 52% for high-risk HIV negative women. Overall, participants were well informed about the purpose and meaning of an anal Pap test, such that 82% (n= 128) correctly identified what part of the body an anal pap tested, 72% (n=113) could identify the purpose of anal Pap test, and 71% (n= 110) correctly understood the meaning of an abnormal anal Pap test (Table 2). Interestingly, 84% (n= 130) of the women reported anal Pap tests either as extremely important or very important for women with HIV. However, knowledge gaps were present when identifying risk factors for HPV- related anal cancer. Only 37% (n= 57) of the sample identified smoking, 56% (n=87) identified anal sex without a condom, 43% (n=67) identified viral infections, and 42% (n=62) identified HIV as risk factors for anal cancer.
Table 2:
Knowledge questionnaire responses by HIV status
| Question1 | Answer Choice *correct answer bolded |
Overall (N=155) N (%) |
HIV positive (n=102) N (%) |
High-risk HIV negative (n=53) N (%) |
P- value2 |
|---|---|---|---|---|---|
| What part of the body does an anal Pap test check? | Don’t know | 11(7) | 7(6.9) | 4(7.5) | 0.153 |
| Vagina | 8(5.2) | 5(4.9) | 3(5.7) | ||
| Anal canal | 130(83.9) | 85(83.3) | 43(81.1) | ||
| Cervix | 8(5.2) | 5(4.9) | 3(5.67) | ||
| What is the purpose of an anal Pap test?3 | Don’t know | 13(8.3) | 7(6.93) | 6(11.32) | 0.821 |
| Check for yeast infection. | 5(3.2) | 3(2.97) | 2(3.77) | ||
| To look inside the butt/bottom. | 19(12.1) | 14(13.86) | 5(9.43) | ||
| To check for anal cancer or abnormal cells. | 113 (72) | 73(72.28) | 38(71.70) | ||
| See why a woman has painful periods. | 0 | 0 | 0 | ||
| Check for cervical cancer. | 6(3.8) | 4(3.96) | 2(3.77) | ||
| To treat cancer. | 0 | 0 | 0 | ||
| What does it mean if you have an abnormal anal Pap test? | Don't know | 22(14.19) | 14(13.73) | 8(15.09) | 0.605 |
| Your female organs look bad. | 5(3.23) | 2(1.96) | 3(5.66) | ||
| You have cancer. | 5(3.23) | 4(3.92) | 1(1.89) | ||
| You have a STD and need antibiotics. | 10(6.45) | 7(6.86) | 3(5.66) | ||
| You have a yeast Infection. | 3(1.940) | 3(2.94) | 0 | ||
| You have abnormal cells that can turn into cancer. | 110(70.97) | 72(70.59) | 38(71.70) | ||
| Section 2: Risk factors associated with anal cancer1 | |||||
| After an abnormal anal Pap test, follow-up may include a blood test:3 | Don’t know | 47(30.32) | 31(30.39) | 16(30.19) | 0.908 |
| Yes | 86(55.48) | 56(54.90) | 30(56.60) | ||
| No | 21(13.55) | 14(13.73) | 7(13.21) | ||
| After an abnormal anal Pap test,follow-up may include a biopsy | Don’t know | 27(17.42) | 12(11.76) | 15(28.30) | 0.908 |
| Yes | 121(78.06) | 86(84.31) | 35(66.04) | ||
| No | 7(4.52) | 4(3.92) | 3(5.66) | ||
| After an abnormal anal Pap test, follow-up may include another Pap test: | Don’t know | 25(16.13) | 15(14.71) | 10(18.87) | 0.027 |
| Yes | 118(76.13) | 77(75.49) | 41(77.36) | ||
| No | 12(7.74) | 10(9.80) | 2(3.77) | ||
| After an abnormal anal Pap test, follow-up may include an anoscopy (An anoscopy is an instrument like binoculars to examine the anal canal very closely) | Don’t know | 34(21.94) | 19(18.63) | 15(28.30) | 0.353 |
| Yes | 116(74.84) | 80(78.43) | 36(67.92) | ||
| No | 5(3.23) | 3(2.94) | 2(3.77) | ||
| After an abnormal anal Pap test, there may be no follow up | Don’t know | 16(10.32) | 11(10.78) | 5(9.43) | 0.947 |
| Yes | 22(14.19) | 14(13.73) | 8(15.09) | ||
| No | 117(75.48) | 77(75.49) | 40(75.47) | ||
| Multiple sex partners make an individual more likely to get anal cancer? | Don’t know | 41(26.62) | 23(22.77) | 18(33.96) | 0.280 |
| Yes | 60(38.96) | 40(39.60) | 20(37.74) | ||
| No | 53(34.42) | 38(37.62) | 15(28.30) | ||
| Not getting an anal Pap test done makes an individual more likely to get anal cancer? | Don’t know | 35(22.58) | 23(22.55) | 12(22.64) | 0.999 |
| Yes | 44(28.39) | 29(28.43) | 15(28.30) | ||
| No | 76(49.03) | 50(49.02) | 26(49.06) | ||
| Using illegal drugs make an individual more likely to get anal cancer? | Don’t know | 39(25.16) | 22(21.57) | 17(32.08) | 0.211 |
| Yes | 30(19.35) | 23(22.55) | 7(13.21) | ||
| No | 86(55.48) | 57(55.88) | 29(54.72) | ||
| Smoking makes an individual more likely to get anal cancer? | Don’t know | 33(21.29) | 18(17.65) | 15(28.30) | 0.294 |
| Yes | 57(36.77) | 40(39.22) | 17(32.08) | ||
| No | 65(41.94) | 44(43.14) | 21(39.62) | ||
| Anal sex without a condom makes an individual more likely to get anal cancer? | Don’t know | 35(22.58) | 23(22.55) | 12(22.64) | 0.501 |
| Yes | 87(56.13) | 60(58.82) | 27(50.94) | ||
| No | 33(21.29) | 19(18.63) | 14(26.42) | ||
| Wrong diet makes an individual more likely to get anal cancer? | Don’t know | 34(21.94) | 15(14.71) | 19(35.85) | 0.001 |
| Yes | 31(20) | 18(17.65) | 13(24.53) | ||
| No | 90(58.06) | 69(67.65) | 21(39.62) | ||
| Sex early in life makes an individual more likely to get anal cancer? | Don’t know | 38(24.52) | 22(21.57) | 16(30.19) | 0.353 |
| Yes | 29(18.71) | 18(17.65) | 11(20.75) | ||
| No | 88(56.77) | 62(60.78) | 26(49.06) | ||
| Weighing too much makes an individual more likely to get anal cancer? | Don’t know | 42(27.10) | 25(24.51) | 17(32.08) | 0.335 |
| Yes | 16(10.32) | 9(8.82) | 7(13.21) | ||
| No | 97(62.58) | 68(66.67) | 29(54.72) | ||
| Viral infections make an individual more likely to get anal cancer? | Don’t know | 51(32.90) | 30(29.41) | 21(39.62) | 0.060 |
| Yes | 67(43.23) | 51(50.00) | 16(30.19) | ||
| No | 37(23.87) | 21(20.59) | 16(30.19) | ||
| Sexually transmitted diseases make an individual more likely to get anal cancer? | Don’t know | 32(20.65) | 19(18.63) | 13(24.53) | 0.356 |
| Yes | 94(60.65) | 66(64.71) | 28(52.83) | ||
| No | 29(18.71) | 17(16.67) | 12(22.64) | ||
| Drinking too much alcohol makes an individual more likely to get anal cancer? | Don’t know | 39(25.16) | 21(20.59) | 18(33.96) | 0.111 |
| Yes | 31(20) | 24(23.53) | 7(13.21) | ||
| No | 85(54.84) | 57(55.88) | 28(52.83) | ||
| Oral sex makes an individual more likely to get anal cancer? | Don’t know | 26(16.77) | 19(18.63) | 7(13.21) | 0.381 |
| Yes | 20(12.90) | 15(14.71) | 5(9.43) | ||
| No | 109(70.32) | 68(62.39) | 41(37.61) | ||
| Abortions make an individual more likely to get anal cancer? | Don’t know | 36(23.23) | 18(17.65) | 18(33.96) | 0.046 |
| Yes | 7(4.52) | 4(3.92) | 3(5.66) | ||
| No | 112(72.26) | 80(78.43) | 32(60.38) | ||
| HIV makes an individual more likely to get anal cancer? | Don’t know | 40(25.81) | 22(21.57) | 18(33.96) | 0.080 |
| Yes | 65(41.94) | 49(48.04) | 16(30.19) | ||
| No | 50(32.26) | 31(30.39) | 19(35.85) | ||
| Can anal cancer be prevented? | Don’t know | 37(23.87) | 25(24.51) | 12(22.64) | 0.375 |
| Yes | 102(65.81) | 64(62.75) | 38(71.70) | ||
| No | 16(10.32) | 13(12.75) | 3(5.66) | ||
| Section 3: HPV knowledge1 | |||||
| What is the human papillomavirus (HPV)? | Don't know | 58(37.42) | 38(37.25) | 20(37.74) | 0.968 |
| Virus acquired from sex that causes warts and cancer. | 86(55.48) | 56(54.90) | 30(56.60) | ||
| Virus acquired from mosquito bite that makes people sick. | 5(3.23) | 4(3.92) | 1(1.89) | ||
| Virus that makes people unable to have children. | 6(3.87) | 4(3.92) | 2(3.77) | ||
| People with HPV are at higher risk for anal cancer: | Don’t know | 67(43.23) | 37(36.27) | 30(56.60) | 0.002 |
| Yes | 68(43.87) | 55(53.92) | 13(24.53) | ||
| No | 20(12.90) | 10(9.80) | 10(18.87) | ||
| People with HIV are at higher risk for anal cancer: | Don’t know | 45(29.03) | 24(23.53) | 21(39.62) | 0.080 |
| Yes | 88(56.77) | 64(62.75) | 24(45.28) | ||
| No | 22(14.19) | 14(13.73) | 8(15.09) | ||
| People with HPV can be cured with medication: | Don’t know | 49(31.61) | 31(30.39) | 18(33.96) | 0.780 |
| Yes | 72(46.45) | 47(46.08) | 25(47.17) | ||
| No | 34(21.94) | 24(23.53) | 10(18.87) | ||
| People with HPV are at higher risk for genital warts: | Don’t know | 47(30.32) | 34(33.33) | 13(24.53) | 0.526 |
| Yes | 92(59.35) | 58(56.86) | 34(64.15) | ||
| No | 16(10.32) | 10(9.80) | 6(11.32) | ||
| People with HPV usually can tell they have it: | Don’t know | 34(21.94) | 23(22.55) | 11(20.75) | 0.863 |
| Yes | 26(16.77) | 18(17.65) | 8(15.09) | ||
| No | 95(61.29) | 61(59.80) | 34(64.15) | ||
| Condoms will keep HPV from spreading: | Don’t know | 25(16.13) | 15(14.71) | 10(18.87) | 0.715 |
| Yes | 100(64.52) | 68(66.67) | 32(60.38) | ||
| No | 30(19.35) | 19(18.63) | 11(20.75) | ||
| Section 4: Attitudes towards HPV vaccination | |||||
| Have you heard about an HPV vaccine? | Don’t know | 9(5.81) | 2(1.96) | 7(13.21) | 0.011 |
| Yes | 61(39.35) | 39(38.24) | 22(41.51) | ||
| No | 85(54.84) | 61(59.80) | 24(45.28) | ||
| How important do you think the HPV vaccine is for preventing anal cancer? | Not sure | 42(27.10) | 21(20.59) | 21(39.62) | 0.009 |
| Extremely important | 51(32.90) | 34(66.67) | 17(33.33) | ||
| Very important | 42(27.10) | 34(33.33) | 8(15.09) | ||
| Somewhat important | 18(11.61) | 13(12.75) | 5(9.43) | ||
| Not at all important | 2(1.29) | 0 | 2(3.77) | ||
| How important is it for men and women with HIV to have regular anal Pap tests? | Not sure | 12(7.74) | 6(5.88) | 6(11.32) | 0.745 |
| Extremely important | 86(55.48) | 59(57.84) | 27(50.94) | ||
| Very important | 44(28.39) | 28(27.45) | 16(30.19) | ||
| Somewhat important | 12(7.74) | 8(7.84) | 4(7.55) | ||
| Not at all important | 1(0.65) | 1(0.98) | 0 | ||
| How important is it for men and women without HIV to have regular anal Pap tests? | Not sure | 18(11.61) | 9(8.82) | 9(16.98) | 0.480 |
| Extremely important | 69(44.52) | 45(44.12) | 24(45.28) | ||
| Very Important | 41(26.45) | 30(29.41) | 11(20.75) | ||
| Somewhat important | 26(16.77) | 17(16.67) | 9(16.98) | ||
| Not at all important | 1(0.65) | 1(0.98) | 0 | ||
Responses dichotomized 0=incorrect/don’t know, 1=correct
Chi-square test
Missing= 1
Anal Cancer Knowledge was significantly associated with HIV status (r=.174, p= .032) and the WIHS recruitment site (r=−.221, p= .006). HIV positive women had a significantly higher mean Anal Cancer Knowledge score than high-risk HIV negative women (t=−2.104, p=.037) and women from the Bronx WIHS site had a significantly higher mean Anal Cancer Knowledge score than women from the Atlanta WIHS site (t=3.262, p=.002).
Knowledge and Attitudes about HPV and the HPV vaccine
The average score of correct responses for HPV Knowledge was 52% for the overall sample; by status, the average score was 54% for HIV positive women and 48% for high-risk HIV negative women. Responses in regards to knowledge about HPV revealed 56% (n= 86) of the women correctly defined HPV. However, less than half of women correctly identified that HPV increased the risk for anal cancer (n=68). Although only 39% (n=62) of women had previously heard of the HPV vaccine, 72% believed the HPV vaccine was important to prevent some cancer, and 62% reported they would likely recommend the HPV vaccine to relatives and friends.
In bivariate analyses, significant correlations to HPV knowledge included history of an abnormal cervical Pap test (r= −.178, p=.029), age (r= −.326, p=.000), history of anal sex (r= −.256, p=.001), smoking status (r=−.176, p=.029); whereas, higher education level (r= .164, p=.042) was correlated with HPV knowledge. Women with a history of an abnormal cervical Pap test (t= 2.137, p=.034) and those age 50 years or younger were more knowledgeable about HPV in the study (t= 3.716, p= .000), as were women who reported a history of anal sex (t= 3.284, p= .001), those with some college education or higher (t= −2.005, p=.047), and non-smokers (t=2.425, p=.016).
DISCUSSION
The women in this study presented with multiple risk factors for anal cancer where almost half were smokers and had previous abnormal cervical Pap tests, the median lifetime sexual partners were >15, and reported a history of a sexually transmitted infection. Despite being a high risk group, there were knowledge gaps regarding risk factors associated with anal cancer and HPV such as smoking and HIV infection. However, most women were knowledgeable about what part of the body an anal Pap tested, the purpose of an anal Pap test, and the meaning of an abnormal anal Pap test.
Anal cancer knowledge did differ by HIV status and WIHS recruitment site. High-risk HIV negative women had lower overall anal cancer knowledge than HIV positive women. This may be due to HIV positive women having higher rates of abnormal cervical cytology thus requiring more diagnostic procedures and therefore more opportunities for provider interaction and patient education [25]. Other studies have found HIV positive women had a better understanding of cervical cancer screening than their negative counterparts [26, 13]. Additionally, women who were recruited from the Bronx WIHS site were more knowledgeable about anal cancer than their Atlanta site counterparts. One possible explanation is that women from the Bronx site are part of WIHS Wave 1 recruitment consortia that enrolled women starting in 1993 (compared to Atlanta’s Wave 4 consortia that began enrollment in 2013). Thus, due to being in the WIHS study longer, women in the Bronx site may have had more opportunity for education.
We found that women with a history of abnormal cervical pap cytology or anal sex, as well as those younger than 50 years old, were more knowledgeable about HPV, regardless of HIV status. Our findings suggest that women at an increased risk for HPV or anal dysplasia, can be offered HPV education or counseling. However, of concern, current smokers were less knowledgeable about HPV; yet, current smoking in women is associated with HPV related anal cancer [27]. Thus, smokers in this sample would benefit from increased HPV education and a smoking cessation intervention. Similar to our findings, prior studies in women with HIV have found that higher education is a significant predictor of greater cervical cancer and HPV knowledge [23, 13]. Thus women with lower education levels are a vulnerable group that would benefit from tailored HPV education interventions. It is important to note that the women in this study were nested in the larger parent WIHS study and undergo cervical pap testing every six months, thus greater opportunities to learn about anal cancer and HPV might have occurred. Thus, HIV positive women from the general population may have lower levels of knowledge and awareness of anal cancer, anal cancer screening, and HPV than reflected in this study.
This study has limitations. It is performed on a group of patients who have frequent visits with the health care system and with regular WIHS related research visits with biannual cervical pap testing; thus, greater involvement and accessibility to resources and clinicians for education. Thus, HIV positive women in the general population may have lower knowledge of anal cancer and HPV than reported in this study. Furthermore, due to the multiple choice nature of the questionnaire, some women may have guessed correctly. Thus, knowledge may be lower than what was measured which is already dismal. Furthermore, study risk factors were extrapolated from self-reported questionnaires that were completed at a different WIHS study visit, thus can limit the strength of relationships. Lastly, we excluded participants who did not speak English, thus limiting applicability of the results to non-English speaking populations. However, this study is one of the few in the literature to report knowledge of anal cancer and its relationship to HPV in a sample of HIV positive and high-risk negative women.
Despite the rising incidence of anal cancer in HIV positive individuals, awareness and knowledge of anal cancer and its association to HPV in HIV positive women is relatively unknown. This study found that although most women were knowledgeable about anal cancer and anal Pap testing, many women showed significant knowledge gaps pertaining to their risk to anal cancer and could not identify major risk factors to anal cancer, such as HIV and HPV infections. Screening for anal cancer is most effective when at-risk populations understand their risk for anal cancer which may motivate cancer screening behaviors. Patient educational interventions are needed to improve knowledge and awareness of HPV and risk for anal cancer.
Acknowledgements:
Data in this manuscript were collected by the Women’s Interagency HIV Study (WIHS). 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). WIHS (Principal Investigators): UAB-MS WIHS (Mirjam-Colette Kempf and Deborah Konkle-Parker), U01-AI-103401; Atlanta WIHS (Ighovwerha Ofotokun and Gina Wingood), U01-AI-103408; Bronx WIHS (Kathryn Anastos and Anjali Sharma), U01-AI-035004; Brooklyn WIHS (Howard Minkoff and Deborah Gustafson), U01-AI-031834; Chicago WIHS (Mardge Cohen and Audrey French), U01-AI-034993; Metropolitan Washington WIHS (Seble Kassaye), U01-AI-034994; Miami WIHS (Margaret Fischl and Lisa Metsch), U01-AI-103397; UNC WIHS (Adaora Adimora), U01-AI-103390; Connie Wofsy Women’s HIV Study, Northern California (Ruth Greenblatt, Bradley Aouizerat, and Phyllis Tien), U01-AI-034989; WIHS Data Management and Analysis Center (Stephen Gange and Elizabeth Golub), U01-AI-042590; Southern California WIHS (Joel Milam), U01-HD-032632 (WIHS I – WIHS IV). The WIHS is funded primarily by the National Institute of Allergy and Infectious Diseases (NIAID), with additional co-funding from the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), the National Cancer Institute (NCI), the National Institute on Drug Abuse (NIDA), and the National Institute on Mental Health (NIMH). Targeted supplemental funding for specific projects is also provided by the National Institute of Dental and Craniofacial Research (NIDCR), the National Institute on Alcohol Abuse and Alcoholism (NIAAA), the National Institute on Deafness and other Communication Disorders (NIDCD), and the NIH Office of Research on Women’s Health. WIHS data collection is also supported by UL1-TR000004 (UCSF CTSA), UL1-TR000454 (Atlanta CTSA), and P30-AI-050410 (UNC CFAR).
U01-AI-103408 (Atlanta WIHS) and UL1-TR000454 (Atlanta CTSA)
U01-AI-035004 (Bronx WIHS)
We would like to acknowledge the National Program of Cancer Registries of the Centers for Disease Control and Prevention (CDC) for the funds that helped support the collection and availability of the cancer registry data and thank the following state cancer registries for their help: AL, CA, FL, GA, IL, MD, MS, NY, NC, and VA. The authors assume full responsibility for analyses and interpretations of these data.
REFERENCES
- 1.Silverberg Michael J., Lau Bryan, Justice Amy C., Engels Eric, Gill M. John, Goedert James J., Kirk Gregory D. et al. 2012. Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clinical Infectious Diseases 54 (7):1026–1034. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Frisch Morten, Biggar Robert J, and Goedert James J. 2000. Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome. Journal of the National Cancer Institute 92 (18):1500–1510. [DOI] [PubMed] [Google Scholar]
- 3.Chin-Hong Peter V., and Palefsky Joel M.. 2005. Human papillomavirus anogenital disease in HIV-infected individuals. Dermatologic Therapy 18 (1):67–76. [DOI] [PubMed] [Google Scholar]
- 4.Palefsky Joel M. a, Holly Elizabeth A., Ralston Mary L., Da Costa Maria, and Greenblatt Ruth M.. 2001. Prevalence and Risk Factors for Anal Human Papillomavirus Infection in Human Immunodeficiency Virus (HIV)-Positive and High-Risk HIV-Negative Women. Journal of Infectious Diseases 183 (3):383–391. [DOI] [PubMed] [Google Scholar]
- 5.Kojic Erna Milunka, Cu-Uvin Susan, Conley Lois, Bush Tim, Onyekwuluje Juanita, Swan David C, Unger Elizabeth R, Henry Keith, Hammer John H, and Overton Edgar T. 2011. Human papillomavirus infection and cytologic abnormalities of the anus and cervix among HIV-infected women in the study to understand the natural history of HIV/AIDS in the era of effective therapy (the SUN study). Sexually Transmitted Diseases 38 (4):253–259. [DOI] [PubMed] [Google Scholar]
- 6.De Vuyst Hugo, Clifford Gary M, Nascimento Maria Claudia, Madeleine Margaret M, and Franceschi Silvia. 2009. Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: A meta analysis. International Journal of Cancer 124 (7):1626–1636. [DOI] [PubMed] [Google Scholar]
- 7.Palefsky Joel M. 2012. Practising high-resolution anoscopy. Sexual Health 9 (6):580–586. [DOI] [PubMed] [Google Scholar]
- 8.Moscicki AB, Darragh TM, Berry-Lawhorn JM, Roberts JM, Khan MJ, Boardman LA, Chiao E et al. 2015. Screening for Anal Cancer in Women. Journal of Lower Genital Tract Disease 19 (3 Suppl 1):S27–42. doi: 10.1097/lgt.0000000000000117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Wells Jessica S, Holstad Marcia M, Thomas Tami, and Bruner Deborah Watkins. 2014. An integrative review of guidelines for anal cancer screening in HIV-infected persons. AIDS Patient Care and STDS 28 (7):350–357. [DOI] [PubMed] [Google Scholar]
- 10.New York State Department of Health. 2007. Primary care approach to the HIV-infected patient. New York: New York State Department of Health. [Google Scholar]
- 11.Palefsky Joel, Berry John Michael, and Jay Naomi. 2012. Anal cancer screening. The Lancet Oncology 13 (7):e279–e280. [DOI] [PubMed] [Google Scholar]
- 12.Fylan Fiona. 1998. Screening for cervical cancer: a review of women's attitudes, knowledge, and behaviour. British Journal of General Practice 48 (433):1509–1514. [PMC free article] [PubMed] [Google Scholar]
- 13.Massad LS, Evans CT, Wilson TE, Goderre JL, Hessol NA, Henry D, Colie C et al. 2010. Knowledge of cervical cancer prevention and human papillomavirus among women with HIV. Gynecologic Oncology 117 (1):70–76. doi: 10.1016/j.ygyno.2009.12.030. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Wigfall LT, Bynum SA, Brandt HM, and Hebert JR. 2016. HPV Vaccine Awareness and Knowledge Among Women Living with HIV. Journal of Cancer Education 31 (1):187–190. doi: 10.1007/s13187-015-0943-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Pitts Marian K, Fox Christopher, Willis Jon, and Anderson Jonathon. 2007. What do gay men know about human papillomavirus? Australian gay men's knowledge and experience of anal cancer screening and human papillomavirus. Sexually Transmitted Diseases 34 (3):170–173. [DOI] [PubMed] [Google Scholar]
- 16.Catania Joseph A, Kegeles Susan M, and Coates Thomas J. 1990. Towards an understanding of risk behavior: An AIDS risk reduction model (ARRM). Health Education Quarterly 17 (1):53–72. [DOI] [PubMed] [Google Scholar]
- 17.Daling Janet R, Madeleine Margaret M, Johnson Lisa Godefroy, Schwartz Stephen M, Shera Katherine A, Wurscher Michelle A, Carter Joseph J, Porter Peggy L, Galloway Denise A, and McDougall James K. 2004. Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer. Cancer 101 (2):270–280. [DOI] [PubMed] [Google Scholar]
- 18.Hessol Nancy A, Holly Elizabeth A, Efird Jimmy T, Minkoff Howard, Schowalter Karlene, Darragh Teresa M, Burk Robert D, Strickler Howard D, Greenblatt Ruth M, and Palefsky Joel M. 2009. Anal intraepithelial neoplasia in a multisite study of HIV-infected and high-risk HIV-uninfected women. Aids 23 (1):59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Holly Elizabeth A, Ralston Mary L, Darragh Teresa M, Greenblatt Ruth M, Jay Naomi, and Palefsky Joel M. 2001. Prevalence and risk factors for anal squamous intraepithelial lesions in women. Journal of the National Cancer Institute 93 (11):843–849. [DOI] [PubMed] [Google Scholar]
- 20.Frisch M, Glimelius B, van den Brule AJ, Wohlfahrt J, Meijer CJ, Walboomers JM, Goldman S, Svensson C, Adami HO, and Melbye M. 1997. Sexually transmitted infection as a cause of anal cancer. New England Journal of Medicine 337 (19):1350–1358. doi: 10.1056/nejm199711063371904. [DOI] [PubMed] [Google Scholar]
- 21.Bacon MC, von Wyl V, Alden C, Sharp G, Robison E, Hessol N, Gange S et al. 2005. The Women's Interagency HIV Study: an observational cohort brings clinical sciences to the bench. Clinical and Diagnostic Laboratory Immunology 12 (9):1013–1019. doi: 10.1128/cdli.12.9.1013-1019.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Barkan Susan E, Melnick Sandra L, Preston-Martin Susan, Weber Kathleen, Kalish Leslie A, Miotti Paolo, Young Mary, Greenblatt Ruth, Sacks Henry, and Feldman Joseph. 1998. The women's interagency HIV study. Epidemiology 9 (2):117–125. [PubMed] [Google Scholar]
- 23.Massad LS, Evans CT, Weber KM, Goderre JL, Hessol NA, Henry D, Colie C, Strickler HD, Watts DH, and Wilson TE. 2010. Changes in knowledge of cervical cancer prevention and human papillomavirus among women with human immunodeficiency virus. Obstetrics and Gynecology 116 (4):941–947. doi: 10.1097/AOG.0b013e3181f2dbae. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Hild-Mosley Katherine A, Patel Dipti M, Markwell Stephen, and Massad L Stewart. 2009. Knowledge of cervical cancer screening, human papillomavirus, and HPV vaccine among Midwestern gynecology patients. Journal of Lower Genital Tract Disease 13 (4):200–206. [Google Scholar]
- 25.Six C, Heard I, Bergeron C, Orth G, Poveda JD, Zagury P, Cesbron P et al. 1998. Comparative prevalence, incidence and short-term prognosis of cervical squamous intraepithelial lesions amongst HIV-positive and HIV-negative women. AIDS 12 (9):1047–1056. [PubMed] [Google Scholar]
- 26.Sichanh Chanvilay, Quet Fabrice, Chanthavilay Phetsavanh, Diendere Joeffroy, Latthaphasavang Vatthanaphone, Longuet Christophe, and Buisson Yves. 2014. Knowledge, awareness and attitudes about cervical cancer among women attending or not an HIV treatment center in Lao PDR. BMC Cancer 14:161. doi: 10.1186/1471-2407-14-161. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Daling JR, Madeleine MM, Johnson LG, Schwartz SM, Shera KA, Wurscher MA, Carter JJ, Porter PL, Galloway DA, and McDougall JK. 2004. Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer. Cancer 101 (2):270–280. doi: 10.1002/cncr.20365. [DOI] [PubMed] [Google Scholar]