Barriers and facilitators of Pap testing for women living with HIV: A focus group study

Cervical cancer is the third most common cancer among women worldwide (International Agency for Research on Cancer, 2015). A report from the landmark prospective cohort study, North American AIDS Cohort Collaboration on Research and Design, involving 13,690 women living with HIV (WLWH) and 12,021 HIV-uninfected women (Abraham et al., 2013), revealed that the cervical cancer incidence rate was higher for WLWH (26 vs. 6 per 100,000 women). Despite increased susceptibility to cervical cancer, WLWH have been less likely to screen for cervical cancer in comparison to uninfected women (58% vs. 81%; Leece et al., 2010; Sauer, Siegel, Jemal, & Fedewa, 2019).

Low cancer knowledge, limited access to care, negative attitudes and beliefs about screenings (e.g., fear of cancer or pain, loss of privacy or embarrassment) have been reported as common barriers to cancer screenings in primarily ethnic minority groups of women without HIV (Adegboyega & Hatcher, 2017; Boom et al., 2018; Forney-Gorman & Kozhimannil, 2016; Ogedegbe et al., 2005). Despite the burden of cervical cancer faced by WLWH, few studies have explored the barriers and facilitators to cervical cancer screening in WLWH. The existing studies revealed that experiences of social rejection, disapproval and discrimination related to HIV diagnoses, and the fear of stigmatization and isolation by male partners may heighten a sense of shame regarding the illness, hence resulting in little motivation to seek appropriate health care and to maintain optimal health (Bateman et al., 2018; Bukirwa et al., 2015; Gagnon, 2015; Kenya et al., 2015; Williams, Moneyham, Kempf, Chamot, & Scarinci, 2015). In contrast, strong provider–patient relationships were reported as factors that positively impacted the health behaviors of WLWH, including cervical cancer screening (Bateman et al., 2018; Fletcher et al., 2014).

Due to the chronic nature of HIV and the unique needs of people living with HIV (PLWH), health promotion programs targeted to PLWH have often been delivered by trained community volunteers or lay educators in close collaboration with HIV care providers (Han et al., 2018). Despite having crucial roles in health promotion programs, the perspectives of those involved in HIV care related to cervical cancer screening have not been explored, but have focused solely on the perspectives of WLWH (Bateman et al., 2018; Bukirwa et al., 2015; Fletcher et al., 2014; Gagnon, 2015; Kenya et al., 2015; Williams et al., 2015). A qualitative study exploring the input of multi-level stakeholders is a way to address this important knowledge gap. Thus, the purpose of our study was to explore the perceptions of WLWH, community advocates, HIV care providers, and relevant frontline personnel, such as community health workers and outreach workers, about barriers and facilitators to cervical cancer screening.

Methods

Design and Sample

Data for our analysis were obtained from focus groups. The focus group is a useful method to identify social norms and expand insight into developing interventions based on needs of the target population (Halcomb, Gholizadeh, DiGiacomo, Phillips, & Davidson, 2007; Morgan, 1997). The inclusion criteria for our study were: (a) ages 18 years and older, (b) able to speak English, (c) WLWH or providers working closely with WLWH, and (d) willing to provide written consent. We attempted to create diverse focus group samples with different education backgrounds and experiences to capture variations and commonalities in relation to views on Pap test screening (Patton, 2002). Potential participants were identified by word-of-mouth and emails to a listserv consisting of faith and community partners in Baltimore, Maryland.

Procedures

The Johns Hopkins Institutional Review Board approved the study. Four focus group interviews were conducted: one with HIV advocates and community volunteers (n = 6), one with HIV care providers (n = 7), and the remaining two with WLWH (n = 6). Each focus group was facilitated by a trained moderator and a note-taker. A focus group guide was developed based on concepts examined during the study period, the literature, and the research team’s experiences. Our study team included researchers, clinicians (a nurse practitioner and a community nurse), an HIV education expert, an outreach coordinator, a community advocate, and study staff who had extensive experience working with PLWH. After discussions with the research team, interview guide questions were revised to increase comprehension by lay persons (see Table 1 for example questions). All focus group interviews were conducted at a community site (HIV clinic or local church) that was most convenient for the participants. Each focus group interview lasted 1 to 1.5 hours. Participants received $30 each for their time. All focus group discussions were audio recorded, transcribed verbatim, and coded using content analysis.

Table 1.

Main Topics and Sample Questions Used in the Semi-Structured Focus Groups

Topic	Sample Questions
Barriers and facilitators for Pap test in women living with HIV	• What factors influence women living with HIV receiving/not receiving Pap smears?
Effectively reaching women living with HIV for Pap testing	• What would be the best way to reach women living with HIV?
Future planning	• What are your thoughts on having an intervention program for women living with HIV to increase their Pap testing?

Data Analysis

Sample characteristic data from a brief survey were analyzed using descriptive statistics such as frequency, percent, and means. Qualitative data from the focus groups were analyzed using inductive coding and qualitative content analysis (Hsieh & Shannon, 2005). Two coders independently read each transcript and field notes multiple times and conducted initial coding. We had 28 to 43 pages of transcript for focus groups; 61% to 91% of the transcripts had to do with discussions directly relevant to Pap smears. Coders then sorted initial codes into categories; emergent categories were grouped into themes. Themes and subthemes were reviewed by other study team members for similarities and discrepancies. Final categories of themes and subthemes were determined after a series of team discussions. Data saturation was reached after four focus group interviews when no new themes emerged. Trustworthiness of the analysis was achieved with multiple methods. Creditability was maximized through the research team’s in-depth experience with WLWH (more than 10 years on average). Transferability was facilitated through thick descriptions of study findings using verbatim transcripts and relevant quotes, thus allowing the reader to judge the applicability of study findings beyond our study. Finally, confirmability was enhanced when the initial coders and co-authors revisited the focus group data (Morse, 2015).

Results

Participants were mostly female (95%), middle-aged (mean = 47.7 years), and African American (79%). Fewer than half (47%) had completed a college or higher level of education. Of the WLWH and community member focus groups, about one third (33%) were college graduates; 71% of the provider group were college graduates. Participants in HIV advocate, community leader, and care provider focus groups averaged more than a decade (mean = 12.3 years) of experience working with PLWH. In focus groups with WLWH, average time living with HIV was 22.7 years (see Table 2).

Table 2.

Characteristics of Focus Group Participants (N = 19)

Characteristics	Value
Age in years, mean	47.7
Female	95%
Black	79%
≥ College graduate	47%
Years working/living with HIV by stakeholder role, mean
HIV advocates/community leaders (n = 6)	15.7
HIV care providers (n = 7)	9.3
Women living with HIV (n = 6)	24.3

Table 3 summarizes key themes and subthemes. The themes were similar across groups, and have been merged for presentation. Themes and relevant quotes from focus groups were categorized as: (a) Barriers to Pap testing in WLWH, (b) facilitators of Pap testing in WLWH, and (c) future planning.

Table 3.

Themes and Subthemes From Focus Groups

Themes	Subthemes	Supporting quotes
Barriers to Pap testing among WLWH	Stigma	“…cause when you say AIDS to the youth; they automatically call you a junkie, you’re going to die, you know all that stuff.” (WLWH) “…they need to be able to talk about women who are still sexually involved, even though they are diagnosed. Because I had a doctor who didn’t tell me to stop having sex, he didn’t tell me I couldn’t get married, he says, as a matter fact, you can still get married, still have babies and all of that. And so because he encouraged me, I think we need to embrace that conversation. That women with HIV are still having sex, still marrying, still having children I think we are afraid to talk about that.” (WLWH) “I’ve encountered people who, once they find out that you are HIV positive, that treat you different. You know it’s like they are afraid to do the swabbing… because I mentioned that I’m HIV positive, or HIV diagnosed, they begin to push this urgency for me to go to a different clinic because they are not comfortable with treating me.” (WLWH)
	Limited health literacy	“The second thing I think that really keeps people in their groove if we are actually talking to them in their language. People begin to stray away when you begin to use terminology that they are not aware of.” (Outreach Worker)
	Competing priorities	“As a woman because you know holding down your household. I’m a full-time student, working full time. And my husband just lost his sight due to his diabetes. I have been literally focused on everybody else.” (WLWH) “How can I take off of work and care of myself because if I lose a day, I don’t get paid.” (HIV Clinician)
	Lack of awareness or knowledge about Pap testing	“Everybody’s walking around like they’re super women. Like nothing’s wrong with me, nothing’s going to happen to me. I don’t have to do this.” (WLWH)
Facilitators of Pap testing among WLWH	Wrap-around support from clinics	“[Our clinic] provides those wrap around services that no other medical facility do, because we really do understand there is a need for those supportive services in order to get to that final point.” (HIV Clinician) “You are going to 1,000 different appointments if you are HIV positive. So let's be proactive. Let's see if we can get everything done on one visit.” (HIV Counselor)
	Good patient-provider relationships	“They smile at us and, ‘Hey I’m glad to see you,’ and it’s not all fake and phony, it’s not about the dollars, they don’t hurry up and rush us out of there because they got a thousand clients… they take their time and talk to people. They don’t hurry up and get you undressed and get your legs up on a table. They actually care about how we feel. You know what I mean? They are actually listening to us, they are paying attention. And it ain't about their quota, their time schedule, it ain't about any of that.” (WLWH)
	Direct encouragement from peers and community members	I think if we can do something like that, have some real life people come in and talk about, you know, someone who might have been diagnosed with cervical cancer, I know for me I would listen to somebody that’s been diagnosed. She could tell me how to prevent being diagnosed, I would listen to that." (WLWH) Word of mouth is what got me in these programs. It’s powerful, especially one-on-one, because a lot of people don’t want to disclose especially if they’re not in an extremely private place they don’t want to talk (Community Advocate)
Future planning	Open group education	“In person is to me, is better than online…in a small intimate, people begin to get intimate with each other in regard to what's really happening.” (Outreach Worker) “Support groups are very good but for me having experience sitting in support groups as well as facilitating them. A lot of people don’t want that textbook of type stuff. Because I don’t want someone sitting in front of me with a book going through and reading it to me. I don’t.” (WLWH)
	Health care provider recommendation of Pap testing	"Doctors need to push more often, explaining to female patients why you need it." (Community Advocate) “I think my gynecologist, she should be aware and say, ‘Ok, even if though this is a female coming to me and this is what I normally deal with. This is a female with HIV so I need to make sure she’s aware and not just assume that I (the patient) am.’ I think she may assume that I’m aware of it.” (WLWH)
	Prevention targeted to younger generation	“Teach them. Cause if we don’t teach them, the street has a way of teaching them, which is all wrong behavior.” (WLWH) “As long as you have an open and honest discussion with your children then, maybe their friends or whatever, they may not have the same parent at home or some guardian that can teach them how to go about screenings.” (WLWH) “You have a situation where you have three generations. A young child, a young mother, and grandmother still under 40. At some point we to stop with that 40 year old and, say, get her to understand that some of the things that she did not do she needs to own them and go to that daughter and teach people the things they need to know and have those conversations making those possible changes easier to occur." (Community Advocate)

Note. WLWH = woman/women living with HIV infection.

Theme 1. Barriers to Pap Testing for Women Living With HIV

Barriers to Pap screening included stigma, limited health literacy, competing priorities, and lack of awareness or knowledge about Pap testing. Participants discussed the stigma in Black communities, faith-based communities, and health care settings. A community advocate and an active member of her ethnic church, shared:

... in the faith-based African American community, they will discuss some cancers… but they will not talk about Pap smears. That’s not something they are going to talk about in the church because, basically, this is a female issue and a lot of churches are hesitant to talk about a female issue.

Limited health literacy in WLWH was a salient barrier when presenting information about Pap testing. The importance of assessing and addressing the health literacy needs of WLWH was highlighted by a community advocate: “If they can’t read or they don’t read well and you give them some reading material, what are they going to do with it? Look at it and pretend that they are reading it.”

Competing priorities often became a barrier to health screenings, as women place fewer emergent concerns such as cervical cancer screening on hold. Participants said that many competing priorities stem from women’s roles as caregivers in a household, placing family members’ needs above their own: “A lot of the times they are trying to deal with child care or caring for another relative,” putting the women’s well-being behind others.

Another significant barrier was a lack understanding about the importance or purpose of Pap tests. An outreach worker noted that messages to women often do not extend past HIV medication adherence, “I think the message now is that people live longer with HIV. That’s the message… just take your meds. Everything else is fine. But they are not thinking about other things that can contribute to their health.”

Theme 2. Facilitators of Pap Testing for Women Living With HIV

Facilitators of Pap testing included wrap-around support from clinics (i.e., non-medical services such as transportation, emergency financial assistance, and substance disorder assistance), strong patient-provider relationships, and peer encouragement. Participants noted that support from clinics should incorporate more diverse social services, making it easier to address multiple health or social needs at once. This, in turn, would help increase Pap testing in WLWH. One HIV care provider noted:

You’re gonna need that psychiatrist or social worker. You’re gonna need every bit of that support within that facility before you walk out the door because most of them are not going to have the support that they need when they walk out the door.

Patient participants noted that strong patient-provider relationships facilitated adherence to health screenings. They explained that close relationships to their providers encouraged them to manage their HIV and obtain health screenings. One woman fondly described the stern, but close, relationship with her doctor:

I love everything about my doctor... She’s not afraid to touch my hand, she’s not afraid to do anything with me...Well, the way my doctor tells me, she be like telling me if I don’t go get tested we [are] gonna fight. She show me tough love.

Direct encouragement from other woman was discussed, as sharing common experiences provided a more powerful and relatable means to communicate the importance of Pap test screening. A WLWH shared,

Someone sitting in front of me telling me, “I understand, I know what you go through, I’ve been there or I’ve had a fear…” Something [like] that connects me to the person… That’ll shake me up and [make me think], “Well dang, maybe I need to go get tested.”

Theme 3. Future Planning

Participants discussed ways in which health promotion programs focused on increasing Pap testing could be designed and delivered. They stated that support groups and health provider discussions were components of future interventions, while noting the importance of reaching out to younger generations for primary prevention of cervical cancer. Participants thought that open group education could facilitate intimate discussion, offer a forum to share experiences, and provide a source of moral support. An HIV clinician, stated:

The group perspective to me is always a wonderful idea because you not only make friends, but you also begin bonding with people that live like you, understand the things that you are going through, and [they are] people that’s outside of your everyday life.

Community members and WLWH highlighted the importance of provider discussions in encouraging and recommending Pap testing, noting that providers should avoid assuming that a patient was comfortable Pap testing or that the patient fully understood the risk of cervical cancer. An outreach worker stated:

I think if providers just acknowledge the fact that it is such a vulnerable, scary thing to do, that would even help because… the way doctors have told me to get Pap smears [is very off the cuff], “Oh you have to get your Pap smear.”

Finally, participants identified cervical cancer prevention targeted to younger women as an important area for future efforts. Participants described a cycle of misinformation and lack of information that increases risk of sexually transmitted diseases and cervical cancer. An HIV clinician explained: “A lot of the behaviors are generational. So, in order for them to begin to break the cycle, they need to be educated about really what is happening in their families.”

Discussion

Focus groups with diverse stakeholders, including WLWH, HIV care providers, HIV counselors, outreach workers, and community advocates, explored the social, economic, and health care factors that may help explain lower rates of Pap testing among WLWH. Participants noted that stigma, limited health literacy, competing priorities, and lack of awareness or knowledge about Pap testing were the main barriers to receiving a Pap test for WLWH.

Research has identified stigma as a major barrier to Pap testing (Gagnon, 2015). Stigma has also been associated with depression and HIV care adherence difficulties (Vanable, Carey, Blair, & Littlewood, 2006). Women can face stigma in many facets of their health; from their HIV status to discussion of gynecological issues and sexual activities (Carr & Gramling, 2004; Gagnon, 2015; Rusch et al., 2008). Stigma can suppress discussion about HIV and gynecologic health by community members and health care providers, discussion that may have otherwise increased awareness of cervical cancer or prompted women to have a Pap test.

Other barriers to screening included limited health literacy, competing priorities, and a lack of understanding about cervical cancer. In particular, limited health literacy was a major barrier addressed by the focus groups. The finding indicated that providers should be cognizant of the differences in comprehension of health information between themselves and their patients. If providers do not present information at an appropriate literacy level, it can hinder patient understanding of cervical cancer screening and may even compromise the provider-patient relationship (McKenna, Sixsmith, & Barry, 2017). Given the low health literacy reported in PLWH, particularly among women, future interventions should address health literacy education as an important component of the intervention (da Cunha, Galvão, Pinheiro, & Vieira, 2017; Dorner, Schulte-Hermann, Zanini, Leichsenring, & Stefanek, 2014).

Wrap-around support, strong patient-provider relationships, and peer encouragement emerged as major facilitators of Pap test screening. A survey of low-income, medically underserved women receiving subsidized gynecologic care through an integrated HIV clinic revealed that access to health care was positively associated with WLWH health behaviors such as cervical cancer screening (Ogunwale et al., 2016). Many federally qualified health centers that treat PLWH provide multiple services such as counseling, transportation, insurance, food, and housing assistance. However, Fletcher et al. (2014) warned that benefits of the “one stop shop” model may be offset by limited health providers, which can cause excessive wait times for services, increasing concerns about missing work and childcare.

A strong provider/patient relationship and the power of meeting and talking with other women were also facilitators of Pap smears for WLWH in our study. Health care providers play vital roles in explaining the importance of Pap testing and can also address concerns that WLWH have about Pap smears. Yet, focus groups in another study revealed that many providers failed to discuss or inquire about cervical cancer screening, thus WLWH did not know that they needed the screening (Andrasik, Rose, Pereira, & Antoni, 2008). Communications between peer women and community members appeared to be a powerful factor in health care decision making; it has been shown to increase awareness, knowledge, and convince other WLWH to engage in health screenings (Ogedegbe et al., 2005). Peer or lay communication may be an optimal way to spread cervical cancer screening information in an effective manner. In disseminating health information, focus group participants described a cycle where young women begin to raise children before they fully understand important aspects of sexual health themselves, perpetuating gaps in knowledge about gynecologic health through subsequent generations. Family members are an important source of trusted information about sex and relationships, and intergenerational education stands as an important tool to establish lasting changes in health behaviors (Han et al., 2018).

Our study had limitations. In particular, four focus groups might be considered low, with one group involving only two participants due to scheduling difficulty. Nevertheless, African American women are disproportionately affected by HIV (Desantis et al., 2016). Therefore, understanding the barriers and facilitators in an appropriate African American context can better tailor interventions toward populations most affected by HIV.

Conclusion

We explored barriers to and facilitators of Pap testing among WLWH using a qualitative approach involving multi-level stakeholders. Future interventions that aim to increase Pap testing by WLWH should address these barriers and facilitators to create effective changes in health behaviors. Provider discussion, support groups, word of mouth, intergenerational education, and consideration of health literacy were identified as potential avenues to successfully reach WLWH in the community. Interventions should also address the importance and purpose of cervical cancer screenings, knowledge about cervical cancer risks, and the stigma that may be associated with HIV and women’s sexual health.