Pap Test Adherence, Cervical Cancer Perceptions, and HPV Knowledge Among HIV-Infected Women in a Community Health Setting

Pap Test Adherence, Cervical Cancer Perceptions, and HPV Knowledge Among HIV-Infected Women in a Community Health Setting Crystal Chapman Lambert, PhD, CRNP, FNP-BC, ACRN, AAHIVS Rasheeta Chandler, PhD, ARNP, FNP-BC Susan McMillan, PhD, ARNP, FAAN Jeffrey Kromrey, PhD Versie Johnson-Mallard, PhD, ARNP, FAAN Don Kurtyka, PhD, MBA, ARNP, FNP-BC, FAANP The Health Belief Model (HBM) has been widely used as a framework to explain health behaviors in diverse populations, but little HBM research has focused on HIV-infected women and their increased risks for cervical cancer. We used Champion’s Health Belief Model and Self-Efficacy scales to assess relationships between Pap test adherence and constructs of the HBM among 300 HIV-infected women. In addition, we assessed the relationship between HPV and cervical cancer knowledge and key HBM concepts. Participants reported low levels of knowledge regarding risk for cervical cancer and HPV. They perceived lower personal risk for cervical cancer. Women with higher perceived self-efficacy and lower perceived barrier scores reported better Pap test adherence. Findings indicate that HIV-infected women are not aware of the risk for cervical cancer and may not take preventive actions. Further research is needed to identify the full range of factors that impact adherence to cervical cancer screening. (Journal of the Association of Nurses in AIDS Care, 26, 271-280) Copyright Ó 2015 Association of Nurses in AIDS Care Key words: Health Belief Model, HIV, HPV, Pap smear, self-efficacy, susceptibility

In a developed country such as the United States, approximately 4,000 women die annually as a result of cervical cancer. HIV-infected women are at increased risk for developing cervical cancer; in fact HIV-infected women are at least five times more likely to develop cervical cancer than the general population (U.S. Department of Health and Human Services [USDHHS], 2013b). Cervical cancer screening is conducted via a Pap test and/or

Crystal Chapman Lambert, PhD, CRNP, FNP-BC, ACRN, AAHIVS, is an Assistant Professor, School of Nursing, University of Alabama at Birmingham, Birmingham, Alabama, USA. Rasheeta Chandler, PhD, ARNP, FNP-BC, is an Assistant Professor, College of Nursing, University of South Florida, Tampa, Florida, USA. Susan McMillan, PhD, ARNP, FAAN, is a Distinguished Professor, College of Nursing, University of South Florida, Tampa, Florida, USA. Jeffrey Kromrey, PhD, is a Professor, College of Education, University of South Florida, Tampa, Florida, USA. Versie Johnson-Mallard, PhD, ARNP, FAAN, is an Associate Professor, College of Nursing, University of South Florida, Tampa, Florida, USA. Don Kurtyka, PhD, MBA, ARNP, FNP-BC, FAANP, is an Assistant Professor, Colleges of Medicine and Nursing, University of South Florida, Director of HIV Services, Tampa General Hospital and Florida Health, Tampa, Florida, USA.

JOURNAL OF THE ASSOCIATION OF NURSES IN AIDS CARE, Vol. 26, No. 3, May/June 2015, 271-280 http://dx.doi.org/10.1016/j.jana.2014.11.007 Copyright Ó 2015 Association of Nurses in AIDS Care

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human papillomavirus (HPV) DNA testing, which can be completed in an office setting on an outpatient basis. However, in 2008 only 60.2% of women ages 21 to 65 years were counseled about Pap tests (USDHHS, 2013b). Although invasive uterine cervical cancer cases remained stable from 2007 through 2009, the goal is to decrease the number of cases from 7.9 per 100,000 to 7.1 cases per 100,000 by 2020 (USDHHS, 2013c). Screening is an essential component of care needed to reach the goal by 2020. In general, 12% to 29% of women are not receiving Pap testing according to the most appropriate guidelines (Denny-Smith, Bairan, & Page, 2006; Peterson, Murff, Cui, Hargreaves, & Fowke, 2008; Tracy, Lydecker, & Ireland, 2010), but the numbers are higher for HIV-infected women. Despite the importance of cervical cancer screening, HIV-infected women’s increased risk for developing cervical cancer, and the insufficient cervical cancerscreening uptake in general, HIV-infected women do not consistently receive cervical cancer screenings according to the most appropriate guidelines. More specifically, 25% to 55% of HIV-infected women had not received an annual Pap test during the previous year (Baranoski, Horsburgh, Cupples, Aschengrau, & Stier, 2011; Oster, Sullivan, & Blair, 2009; Simonsen et al., 2014; Tello et al., 2010). Given these numbers, we developed a study of HIV-infected women guided by the Health Belief Model (HBM), using Champion’s revised Health Belief Model (CHBM) scale, Champion’s SelfEfficacy (CSE) scale, and HPV and cervical cancer knowledge. The purpose of our study was to evaluate the relationships between Pap test adherence during the previous year and the following variables: HPV and cervical cancer knowledge, and perceived susceptibility, perceived seriousness, perceived barriers, perceived benefits, and perceived self-efficacy.

Cervical Cancer The cervix is the portion of the uterus that connects the body of the uterus to the vagina (American Cancer Society, 2014). Cervical cancer is commonly caused by HPV. There are more than 150 types of HPV, and 40 of those types can affect cells of the genitals; types 16 and 18 are responsible for the majority

of cervical cancer cases (National Cancer Institute, 2013). After HPV infection, cells gradually develop into precancerous cells and, when left untreated, the cells have the potential to develop into cancer. The process varies for each woman, and not all women infected with HPV develop cervical cancer; for many women, the precancerous cells will resolve without treatment (American Cancer Society, 2014; National Cancer Institute, 2013). HPV is transmitted during sex (vaginal, anal, and oral) via skin-to-skin contact (National Cancer Institute, 2013). All sexually active individuals are at risk for HPV, and 42.5% of women will have genital HPV at some point. Tobacco use, having a weakened immune system such as HIV infection, multiparity, chronic inflammation caused by infection with chlamydia, and long-term oral contraceptive use increase the risk of developing cervical cancer (National Cancer Institute, 2013). Women can prevent HPV by remaining abstinent from all sexual activity. Women who are sexually active can reduce the risk of being infected with HPV by remaining in a mutually monogamous relationship with an uninfected partner, using condoms properly, and receiving one of two Food and Drug Administration-approved HPV vaccines (National Cancer Institute, 2013). HIV-infected women are at greater risk for HPV infection and, ultimately, for cervical cancer, because the body’s ability to fight infection is reduced as a result of a weakened immune system (American Cancer Society, 2014). The advent of antiretroviral therapy has transitioned HIV disease from an acute illness to a chronic illness and increased life expectancy among individuals infected with HIV, but antiretroviral therapy has not decreased infected women’s susceptibility to cervical cancer. Current cervical cancer screening recommendations for HIV-infected women are as follows: HIV-infected women should receive Pap testing every 6 months for 1 year after diagnosis and annually thereafter (American College of Obstetrics and Gynecology, 2010; USDHHS, 2013a). Despite increased risk, HIV-infected women often do not receive Pap testing per the aforementioned recommendations (Baranoski et al., 2011; Oster et al., 2009; Simonsen et al., 2014; Tello et al., 2010). Researchers have assessed Pap test adherence in various groups of women, but no studies

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were found that used the concepts of the HBM measured by CHBM and CSE scales to assess Pap test adherence in HIV-infected women. Conceptual Framework Historically, in behavioral science research, the HBM has been used to explain preventative health behaviors such as the actions taken to prevent, screen for, and control illness (Glanz, Rimer, & Viswanath, 2008; Rosenstock, 1966, 1974a). The HBM has been used to explain behaviors such as tuberculosis screening, cancer screening, and risky sexual behaviors (Champion, 1984, 1999; Glanz et al., 2008; Guvenc, Akyuz, & Acikel, 2011; Rosenstock, 1966, 1974a). The constructs of the original HBM include perceived susceptibility, perceived seriousness, perceived benefits, and perceived barriers to a specific behavior, with the addition of cues to action and health motivation in the 1970s and perceived selfefficacy in 1988 (Rosenstock, 1974b; Rosenstock, Strecher, & Becker, 1988). The model suggests that a person’s beliefs, attitudes, and perceptions about a disease determine their actions to seek methods to prevent, screen for, and control a disease (Rosenstock, 1974a, 1974b). Intrapersonal factors such as knowledge, socioeconomic issues, and age influence health behaviors (Rosenstock, 1974b). Therefore, intrapersonal factors modify an individual’s perceptions of susceptibility to disease, seriousness of disease, benefits to prevention, barriers to prevention, and selfefficacy, which ultimately influence an individual’s health promotion and disease prevention behaviors. Several studies have assessed the relationship between HBM variables and cancer screening using the CHBM and CSE scales (Champion, 1993; Champion, Skinner, & Menon, 2005; Denny-Smith et al., 2006; Guvenc et al., 2011; Ingledue, Cottrell, & Benard, 2004). Few studies have assessed the relationship between HBM variables and cervical cancer screening (Denny-Smith et al., 2006; Ingledue et al., 2004; Montgomery, Bloch, Bhattacharya, & Montgomery, 2010). Ingledue and colleagues (2004), Denny-Smith and colleagues (2006), and Montgomery and colleagues (2010) explored HPV and cervical cancer knowledge, and health beliefs related to cervical cancer and cervical cancer screening in samples of college women,

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women enrolled in nursing school, and older women, respectively. Although the studies assessed health beliefs such as perceived susceptibility and perceived seriousness, the studies did not assess perceived benefits, perceived barriers, or perceived self-efficacy. Therefore, our study is the first to use CHBM and CSE scales to evaluate cervical cancer and cervical cancer screening beliefs and attitudes in HIVinfected women. The CHBM scale measures perceived barriers, perceived benefits, perceived susceptibility, and perceived seriousness; the CSE scale measures perceived self-efficacy.

Methods Design The study was an exploratory, cross-sectional, quantitative correlational design. Sample and Setting A convenience sample consisting of 300 HIVinfected women was recruited from two HIV ambulatory care clinics located in Florida. Inclusion criteria were as follows: participants had to be women, 18 years of age or older, and patients at one of the clinics. Women with a history of having had a hysterectomy and women who could not read and comprehend the English language were excluded from the study. Power analysis was conducted to estimate sample size. A power analysis for multiple logistic regression was conducted assuming power 5 .80, a 5 .05, and an odds ratio of at least 2 indicated the need for a sample size of 276. We oversampled by 24 participants to account for missing data in the event that a small percentage of the participants elected not to answer every question. Instruments The questionnaire for the study consisted of six subscales and demographic questions. The principal investigator developed the demographic questionnaire. The demographic questionnaire consisted of 20 questions and was segmented into parts; part one was a medical record (paper chart) review completed

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by the principal investigator, and part two was a survey completed by the participant. For example, participants were asked questions regarding age (not date of birth), race/ethnicity, marital status, primary language, education level, cigarette use, substance use, and Pap test history. The questions were selected based on the review of related literature. Champion’s Health Belief Model. Perceived susceptibility, perceived seriousness (severity), perceived benefits, and perceived barriers were measured using an adapted version of the CHBM scale for cervical cancer and Pap test. The CHBM scale consisted of four subscales (Champion, 1984). The four subscales, totaling 28 items, were measured with a 5-point Likert-type scale ranging from strongly agree to strongly disagree (Champion, 1999; Guvenc et al., 2011). Reported internal consistency for perceived susceptibility, seriousness, and barriers was at least .70 in three studies (Champion, 1984; Guvenc et al., 2011; Medina-Shepherd & Kleier, 2010). Internal consistency for perceived benefits varied, ranging from .62 to .80. Test-retest reliability coefficients for perceived benefits, barriers, seriousness, and susceptibility ranged from .65 to .88. Construct validity for perceived benefits, barriers, seriousness, and susceptibility was examined by factor analysis, and most of the items loaded on their perspective factors at .35 and higher (Champion, 1984, 1999; Guvenc et al., 2011; Medina-Shepherd & Kleier, 2010). In our study, internal consistency as measured by Cronbach’s alpha was .92 for perceived susceptibility scale, .85 for perceived seriousness, .72 for perceived benefits, and .89 for perceived barriers. All of the scales had high reliability except the perceived benefits scale, which was acceptable, indicating that the scales measured the intended constructs (George & Mallery, 2006). Self-efficacy. Self-efficacy (confidence) was measured using Champion’s Self-Efficacy (CSE) scale, which consisted of 10 questions (Champion et al., 2005). The scale was measured with a 5-point Likertlike scale ranging from strongly agree to strongly disagree. The CSE scale has not been widely used in research. The scale has a Cronbach’s alpha of .87 and a Pearson’s coefficient of .52 for test-retest reliability. For our study, the Cronbach’s alpha for perceived self-efficacy was .92, indicating high reliability.

Knowledge. HPV and cervical cancer knowledge was measured by 15 multiple-choice questions. The questionnaire, originally developed by Ingledue and colleagues (2004), consisted of 40 items measuring HPV and cervical cancer knowledge, perception, and prevention behaviors. The first 15 items, measuring HPV and cervical cancer knowledge, were used. Each question had one correct response. The possible range of scores was from 0 to 15; higher scores equated to more knowledge about HPV and cervical cancer (Denny-Smith et al., 2006; Ingledue et al., 2004). Content validity for the knowledge portion of the test was determined by a panel consisting of two gynecologists, two professors of health education, and a medical professional from the Breast and Cervical Program (Ingledue et al., 2004). Test-retest reliability for knowledge was .90 (Ingledue et al., 2004). For our study, Kuder-Richardson-20 (KR20) was used to determine internal consistency of the HPV and cervical cancer knowledge scale; the KR20 was .81, indicating high reliability. Data Collection Data collection began after the Florida Department of Health’s Institutional Review Board approved the study. Participants were recruited from the waiting rooms of two local ambulatory HIV care clinics. To reduce the risk to participant anonymity, the researcher requested a waiver of documentation of consent because the consent form would be the only document to identify participants by name. Each participant was given an informed consent cover letter, a survey, and an envelope. The informed consent cover letter informed participants that their involvement was voluntary and would not influence the care they received. Participants implied consent to the study by completing the survey. Each survey was assigned a unique identifier, which was written on the top of both surveys. The unique identifier allowed the researcher to match the participant’s completed survey to the chart review questionnaire. Data collection occurred in two phases. Phase one consisted of a self-administered survey completed by the participant. The survey could be completed in 45 minutes or less. Phase two consisted of a review of the participant’s chart by the researcher. The chart review was completed while the participant was

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completing the self-administered survey. After completing the questionnaire, the participant showed the survey to the researcher, who reviewed it for completeness. If the questionnaire was not complete, the participant was given an opportunity to answer any incomplete questions. At that time, the researcher gave the participant a gift card containing $15 (USD) as an incentive for participating in the study. The survey was placed in an envelope and locked in a cabinet in a secured office. In addition, completed surveys were scanned and saved to a password-protected flash drive. Data Analysis The data were analyzed using SPSS statistical software (Version 21; IBM, Armonk, NY). Descriptive statistics were used to describe sample characteristics and Pap test adherence. Means and standard deviations were calculated for perceived susceptibility, perceived seriousness, perceived barriers, perceived benefits, perceived self-efficacy, and HPV and cervical cancer knowledge. Pearson’s correlation coefficients were calculated to assess the relationship within the HBM variables. Analysis of variance (ANOVA) was used to determine whether mean differences existed for perceived susceptibility, perceived seriousness, perceived barriers, perceived benefits, perceived self-efficacy, and HPV and cervical cancer knowledge between women who reported having had a Pap test during the past year and women reporting not having had a Pap test during the past year and to obtain h2. Multiple logistic regression was used to determine whether perceived susceptibility, perceived seriousness, perceived barriers, perceived benefits, perceived self-efficacy, and HPV and cervical cancer knowledge predicted cervical cancer screening adherence.

Results Descriptive The sample consisted of 300 participants who were recruited from two (one rural and the other metropolitan) ambulatory HIV care clinics in Florida. Participants reported their race as Black/African American (68%), Hispanic-Latina (14%), Caucasian (16.3%), or other (1.7%). The women reported their levels of

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education as high school or vocational education (50.3%), less than a high school education (33%), or college educated (16.7%). The participants’ ages ranged from 18 to 70 years, with a mean age of 45.4 (SD 5 11; see Table 1). Eighty percent of the women were recruited from a metropolitan HIV ambulatory clinic and 20% from a rural HIV ambulatory clinic. Seventy-five percent of the women reported having a Pap test during the previous year; however, according to the medical record, approximately 44% of the women had had a Pap test at the clinic during the previous year. One reason for the reported and observed differences in Pap test utilization could be that some of the participants had received Pap testing from an outside health care provider. The constructs of HBM were evaluated using several subscales. The perceived susceptibility subscale consisted of four items measuring women’s perceived susceptibility to cervical cancer. Perceived susceptibility scores were low, indicating that, on average, the women did not perceive that they were susceptible to cervical cancer. The perceived seriousness subscales consisted of seven items measuring women’s perceptions of the severity of cervical cancer, and women in this study did not perceive that cervical cancer was serious. The perceived benefits subscale consisted of four items measuring women’s perceptions of the benefits of Pap testing. Perceived benefits scores were high, indicating that women in our study perceived Pap testing as beneficial. Champion’s perceived barriers subscale consisted of 14 items measuring women’s perceived barriers to obtaining Pap testing. Perceived barriers scores were low, indicating that the women did not perceive barriers to obtaining Pap testing. The HPV/cervical cancer knowledge scale consisted of 15 items measuring women’s knowledge of HPV and cervical cancer. For example, participants were asked multiple-choice questions such as the route of transmission for the virus that caused cervical cancer, the virus that caused genital warts, and methods to prevent cervical cancer. In addition, participants were asked true-and-false questions regarding risk factors for cervical cancer. Knowledge scores were low, indicating that the women were not aware of risk factors for HPV and cervical cancer (Table 1). The purpose of our study was to evaluate the relationships between Pap test adherence in women

276 JANAC Vol. 26, No. 3, May/June 2015 Table 1.

Means and Standard Deviation for Subscales and Age

Variables Age Perceived susceptibility Perceived benefits Perceived seriousness Perceived self-efficacy Perceived barriers Knowledge

Table 2.

Range Mean Standard Deviation 18–70 4–20 4–20 7–35 10–50 14–56 0–14

45.4 9.59 15.93 20.88 40.22 29.16 6.02

11.00 4.06 3.20 6.12 6.98 9.09 3.59

Note: n 5 300.

infected with HIV and the following variables: perceived susceptibility, perceived seriousness, perceived benefits, perceived barriers, perceived self-efficacy, and the HPV and cervical cancer knowledge scale. Pearson’s correlation coefficient and ANOVA were used to evaluate the aforementioned relationships. In addition, the researchers wanted to test the ability of the HBM, measured by the CHBM and CSE scales, and HPV and cervical cancer knowledge to predict Pap test adherence among HIV-infected women using logistic regression. Pearson’s correlation coefficient was used to assess the relationship between perceived susceptibility, perceived seriousness, perceived benefits, perceived barriers, perceived self-efficacy, and HPVand cervical cancer knowledge. Statistically significant correlations existed between knowledge and perceived selfefficacy, r(300) 5 .30, p , .01; knowledge and perceived barriers, r(300) 5 2.18, p , .01; and knowledge and perceived benefits, r(300) 5 .16, p , .01. As perceived seriousness increased, perceived susceptibility, perceived benefits, and perceived barriers increased, r(300) 5 .37, p , .01; r(300) 5 .13, p , .05; and r(300) 5 .30, p , .01, respectively. A strong correlation existed between perceived selfefficacy and perceived benefits, r(300) 5 .53, p , .01. Perceived susceptibility and perceived barriers were weakly correlated, r(300) 5 .28, p , .01. In addition, the researchers wanted to test the ability of perceived susceptibility, perceived seriousness, perceived benefits, perceived barriers, perceived selfefficacy, and HPV and cervical cancer knowledge to predict Pap test adherence in HIV-infected women. A one-way ANOVA examined differences in subscale variables by participants who reported having and participants who reported not having a

Differences in Subscale Scores by ParticipantReported Pap Test M

Pap ,1 year .1 yearb Susceptibility ,1 yeara .1 yearb Seriousness ,1 yeara .1 yearb Benefits ,1 yeara .1 yearb Barriers ,1 yeara .1 yearb Self-efficacy ,1 yeara .1 yearb Knowledge

a

5.89 6.39 9.65 9.38 20.63 21.59 16.05 15.55 27.96 32.67 40.73 38.71

SD

F

df

3.74 1.11 (1,298) 3.08 4.23 0.26 (1,298) 3.51 6.37 1.40 (1,298) 5.28 3.23 1.40 (1,298) 3.07 9.01 15.95 (1,298) 8.46 7.32 4.83 (1,298) 5.60

p

h2

.293 .004 .611 .001 .239 .005 .239 .005 .000 .051 .029 .016

Note: na 5 224, nb 5 76.

Pap test during the previous year. No significant differences were found between participants on the subscale variables of knowledge, perceived susceptibility, perceived seriousness, and perceived benefits. Women who reported having had a Pap test during the previous year perceived fewer barriers (p # .001) and higher self-efficacy (p 5 .029) than women who reported having had a Pap test more than 1 year ago (Table 2). The HBM has been used to predict health behaviors, and the CHBM and CSE scales have been used to predict cancer screening. Based on the current literature, we included the following variables in the model: perceived susceptibility, perceived seriousness, perceived benefits, perceived barriers, perceived self-efficacy, and HPV and cervical cancer knowledge. Logistic regression was used to estimate the ability of the constructs of the HBM and HPV and cervical cancer knowledge to predict Pap testing adherence in HIV-infected women (Table 3). Perceived barriers and perceived susceptibility were significant predictors of self-reported Pap test adherence. The overall predictive model was statistically significant (likelihood c2 5 24.58, df 5 8, p , .01). The probability of adhering to Pap testing during the previous year was contingent upon the perceived barriers level. Women with higher barriers scores were less likely to adhere to annual Pap testing. Women who felt more susceptible to cervical cancer were more likely to adhere to annual Pap testing. Overall, perceived susceptibility and

Lambert et al. / Pap Test Adherence, Cervical Cancer Perceptions, and HPV Knowledge Table 3.

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Multivariate Logistic Regression

Model

B

SE

Wald’s

p

OR

Susceptibility Seriousness Benefits Barriers Self-efficacy Knowledge Constant

.083 2.015 .027 2.068 .017 2.08 1.157

.041 .026 .052 .019 .027 .043 1.518

3.97 .321 .266 12.21 .385 3.80 .581

.04 .57 .61 ,.01 .54 .05 .45

1.086 .985 1.027 .934 1.017 .920 3.180

95% CI for OR Lower Upper 1.001 .936 .928 .902 .964 .846

1.178 1.037 1.137 .972 1.073 1.00

OR 5 odds ratio; CI 5 confidence interval. Note: Adjusted for age (continuous), education level (less than high school vs. high school vs. college), and race (Black vs. White).

perceived barriers accounted for 11% of the variance (Nagelkerke R2 5 .116). The overall predictive accuracy of the model was 76%.

Discussion Understanding HIV-infected women’s perceptions and knowledge about cervical cancer screening and HPV is essential to developing a culturally appropriate and effective intervention aimed at increasing Pap test adherence and awareness among women infected with HIV. The purpose of our study was to use constructs of the HBM to assess Pap test adherence in HIV-infected women receiving health services in a community health setting. Pap test nonadherence rates among women in our study were higher than previously reported rates in HIV-infected women (Baranoski et al., 2011; Oster et al., 2009; Simonsen et al., 2014; Tello et al., 2010). This finding may reflect a lack of awareness of personal susceptibility, barriers to health services, or lack of awareness about cervical cancer, Pap testing, and HPV. The HPV and cervical cancer knowledge scores of the women in our study were low, and the mean score was lower than mean scores in other studies with a similar sample size (Denny-Smith et al., 2006; Ingledue et al., 2004; Montgomery et al., 2010). The data suggest that these women may be confused about the purpose of Pap testing and their risks for HPV and cervical cancer. The women were either not receiving information about cervical cancer, Pap test, or HPV during their health care visits or they did not retain and act on the information. Further analysis is essential to determine knowledge areas

that were weak. In addition, health care providers can take advantage of each visit as an opportunity to inform women about the importance of cervical cancer screening and risk factors for HPV and cervical cancer. Following the example of retention in HIV care researchers, clinics can hang signs in exam rooms, waiting rooms, and along clinic hallways to increase awareness, knowledge, and, potentially, Pap test adherence (Raper, 2014). Although not all concepts were statistically related to Pap test adherence, perceived barriers and self-efficacy were significantly related, indicating that differences in Pap test adherence existed for the women who perceived fewer barriers and higher perceived self-efficacy. Previous studies have concluded similar results regarding the relationship between perceived barriers and Pap test adherence in women who were not HIV-infected, but the studies did not measure perceived self-efficacy (Ben-Natan & Adir, 2009; Boonpongmanee & Jittanoon, 2007; Lee, Fogg, & Menon, 2008; Tracy et al., 2010). Several studies reported significant differences between Pap test adherence and the remaining concepts of knowledge, and perceived benefits, susceptibility, and severity, for women not infected with HIV (Burak & Meyer, 1997; Ingledue et al., 2004; Tracy et al., 2010). Boonpongmanee and Jittanoon (2007) reported significant differences in perceived benefits and barriers between Taiwanese women who had a Pap test and women who denied having a Pap test; Burak and Meyer (1997) reported similar results in female students at a New England state college; and Ben-Natan and Adir (2009) reported similar results among Israeli lesbian women. In a sample of women who self-identified as lesbian, routine screeners perceived fewer barriers and more benefits to Pap

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testing, and nonroutine screeners felt more susceptible to cervical cancer (Tracy et al., 2010). Using the same HPV and cervical cancer knowledge scale, Ingledue and colleagues (2004) reported that women attending a U.S. Midwestern university who had had a Pap test during the previous 12 months were more knowledgeable about HPV and cervical cancer. Denny-Smith and colleagues (2006) reported the same results among female college students at a U.S. Southeastern university. The relationship between knowledge and Pap test adherence was not significant in our study, however. The ability of the HBM to explain Pap test adherence varies in different populations. Our study provides evidence that there are relationships between perceived barriers, perceived self-efficacy, and Pap test adherence in HIVinfected women, which suggests that reducing barriers and increasing women’s perceived self-efficacy has the potential to increase the likelihood that HIVinfected women will adhere to Pap testing. The data suggest a directional relationship not implying causality. Perceived susceptibility was also a significant predictor of Pap test adherence for our participants, indicating that the women who perceived increased susceptibility to cervical cancer were nine times more likely to adhere to Pap testing than women who did not perceive that they were susceptible to cervical cancer. Therefore, the aforementioned data and the low mean perceived susceptibility score highlight the need to increase HIV-infected women’s awareness of their personal risks for HPV and cervical cancer. As in our study, perceived barriers have been found to be a robust predictor of annual Pap test adherence (Boonpongmanee & Jittanoon, 2007; Burak & Meyer, 1997; Lee et al., 2008; Tracy et al., 2010). However, Burak and Meyer (1997) found that increased perceived benefits and fewer perceived barriers were significant predictors of Pap testing, and Tracy and colleagues (2010) found that knowledge of screening guidelines, perceived benefits, and perceived barriers were significant predictors of Pap testing among women who self-identified as lesbian. In our study, overall knowledge scores were low (M 5 6.02, SD 5 3), which could contribute to failure of knowledge to predict Pap test adherence. These results suggest that the ability of the HBM to predict behaviors varies depending on the population being evaluated. Further research in HIV-infected women should include HPV and cervical cancer knowledge

as part of an intervention to increase Pap test adherence, perceived self-efficacy, and perceived barriers, despite the insignificant relationship to Pap adherence in our study. We used the constructs of the HBM to explore cervical cancer screening among HIV-infected women. Although the model has been used to explain cervical cancer screening in women not infected with HIV, it is likely that other factors may have influenced the cervical cancer screening behaviors of HIV-infected women who were not included in the model. In addition, the HBM may fail to capture unique factors associated with health behaviors in the African American community, and approximately 68% of the participants in our study identified as being African American or Black (Cochran & Mays, 1993). Future research should employ culturally sensitive theories to guide research in minority communities. Limitations Particular limitations should influence the interpretation of our study findings. First, the majority of participants lived in a metropolitan area and all participants received care at a Ryan White Program-Funded facility. In addition, we did not capture HIV-infected women not in care who were also at increased risk for acquiring HPV and developing cervical cancer. Finally, our convenience sampling method limits generalizability to other women infected with HIV. The study does, however, provide suggestions for future studies and extends the existing body of literature. Implications for Practice In practice, the rationale for procedures and results must be explained to arm patients with the knowledge needed to promote behaviors that decrease cancer risk. In addition, the provider should provide information in a way that patients can understand, and the provider should ask the patient to repeat the information to assess the patient’s level of comprehension. The results of our study suggest that many women lack information regarding HPV and cervical cancer. There are many possible reasons for low HPV and cervical cancer knowledge, including missed opportunities to teach due to the complexity of ambulatory HIV care visits. It is essential for providers to remain

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abreast of current health care guidelines to improve patient outcomes, educate patients, and decrease health care costs. Most importantly, health professions curricula must emphasize keeping up with the latest research and patient care guidelines and the importance of providing patient-centered education as ways to ensure the best health outcomes.

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assess the HPV and cervical cancer knowledge of health care providers because patients may be unaware because their providers are unaware. Health care providers must remain competent, build strong relationships with their patients, reduce barriers, and increase health awareness to promote patient self-care management with the purpose of improving health outcomes and cost effectiveness.

Implications for Research Our findings suggest that similar studies should be repeated (a) in rural areas and private clinics, (b) with HIV-infected women who are not in care, and (c) on the cultural components of care for African American women. Future studies should also address the utility of mobile Pap screenings in underserved areas and the use of telemedicine with the option to perform self-sampling or self-administered Pap tests. Future research is essential to better understand HIV-infected women’s attitudes, perceptions, and knowledge regarding HPV, cervical cancer, and Pap testing. Future studies assessing the relationships between factors such as perceived barriers, perceived susceptibility, perceived self-efficacy, and HPV and cervical cancer knowledge are essential prior to intervention development. Our study highlighted the finding that chronic diseases such as HIV can impact health behaviors in ways that are currently not well understood. Pilot studies are, therefore, essential prior to implementing interventions for individuals impacted by chronic diseases if those interventions were developed for healthy individuals. In addition, future studies should assess health care providers’ knowledge of HIV, HPV, and cervical cancer. Last, future interventions with the goal of increasing awareness and adherence, and improving health care outcomes for HIV-infected women are essential.

Conclusion Despite the inability of CHBM, in its entirety, to explain Pap test adherence in HIV-infected women, many of the concepts have important implications for health care and future research. The increased risk of the population coupled with low HPV and cervical cancer knowledge indicates a need for more HPV education. In addition, it suggests the need to

Key Considerations  Current guidelines recommend that HIVinfected women receive Pap tests annually.  Office visits are missed opportunities to increase Pap test uptake.  HIV-infected women lack knowledge regarding cervical cancer and HPV, creating a teaching opportunity for providers.  Although the Health Belief Model has been widely used, it is likely that other factors not included in the model may be influencing cervical cancer screening behaviors.

Disclosures The authors report no real or perceived vested interests that relate to this article that could be construed as a conflict of interest.

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