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Abstract

Introduction:

Populations at risk for HIV infection—including gay, bisexual, and other men who have sex with men (GBM) and transgender/gender diverse people (TGD)—are at disproportionate risk for anal cancer. Most anal cancers are caused by human papillomavirus (HPV) and are preventable with HPV vaccination and screening. Engaging at-risk populations who are already receiving HIV preventive care (eg, pre-exposure prophylaxis [PrEP]) may be an effective implementation strategy. The purpose of this study was to (1) identify the information, motivation, and behavioral skills that influence decisions about anal cancer prevention and to (2) describe the healthcare utilization patterns among PrEP users that impact their engagement in anal cancer prevention.

Methods:

Using purposive sampling in the United States, we ensured diverse representation among PrEP users aged 18 to 45 across gender and ethnoracial identities. Recruitment sources included primary healthcare clinics, social media, and community venues. Semi-structured interviews were recorded, transcribed, and coded using structural, pattern, and theoretical approaches.

Results:

Participants (N = 36) were mostly cisgender gay ethnoracial minority men. We identified 29 unique codes that were nested within 3 categories: individual decision-making, healthcare utilization patterns, and healthcare system influences. Participants commonly lacked essential information about HPV and anal cancer, often holding misconceptions about risks and prevention. Motivation for anal cancer prevention was driven by healthcare interactions and perceived risks, while fragmented healthcare and reliance on telemedicine were potential barriers. Many participants used telehealth services to access PrEP, described it as convenience, cost-effective, and liked the lack of provider interaction. Some participants used telehealth for PrEP and did not have a primary care provider. The importance of access to LGBTQ+-affirmative healthcare services was highlighted.

Conclusions:

Integrating patient education and prevention services into ongoing PrEP management can enhance the reach and equity of anal cancer prevention. Our model underscores critical areas of misinformation, necessary systems-level changes, and unmet needs.

Keywords

immunization minority group non-heterosexual persons sexual minorities Black Americans Latinx Americans sexually transmitted infections

Introduction

The synergistic relationship between oncogenic human papillomavirus (HPV), concurrent sexually transmitted infections (STIs), and sexual behavior (eg, receptive anal intercourse) contributes to a syndemic of anal cancer risk disproportionally impacting gay, bisexual, and other men who have sex with men (GBM) and transgender/gender diverse (TGD) persons at risk for HIV.¹ The necessary and sufficient cause of anal cancer is oncogenic anal HPV infection.² However, concurrent STIs, including syphilis and gonorrhea, increase the risk of anal cancer in the presence of persistent HPV infection.² Anal cancer risk is greatest for GBM living with HIV (~85/100 000 person-years).³ But HIV-negative GBM are the largest at-risk population given the incidence rate (~19/100 000 person-years) and population size.³ TGD, such as transgender women, have similar if not greater risk of precancerous anal lesions than GBM, but data on anal cancer incidence in this population is not avaiable.⁴

These disparities have been well established, but information about anal cancer risk and prevention has not been widely disseminated to these at-risk groups. In studies spanning nearly 20 years, awareness of anal cancer—including knowledge that HPV infection causes anal cancer and that anal cancer can be prevented by HPV vaccination—is low among GBM.^5
-10 Lack of patient education in this area limits the uptake of anal cancer prevention strategies, such as HPV vaccination and anal cancer screening, thus perpetuating anal cancer disparities.

HPV vaccination is safe and effective at preventing oncogenic anal HPV infection.^11,12 It is currently licensed in the United States for adults up to age 45 and indicated for the prevention of anal cancer.¹³ If not vaccinated at ages 11 or 12, catchup vaccination is recommended for all adults up to the age of 26 and shared clinical decision-making for HPV vaccination is recommended for adults aged 27 to 45.¹⁴ Coverage among adolescent males in the general population of the United States is currently insufficient (~60%) to reduce anal cancer disparities.¹⁵ There are significant inequities in HPV vaccination initiation across social strata defined by gender identity, race/ethnicity, and sexual orientation.¹⁶ Most recent estimates in the United States are that HPV vaccine initiation was just 33% among GBM aged 18 to 26 and 13% among those 27 years and older.¹⁷ Uptake is even lower among Black and Hispanic GBM and largely unknown for GDP.^17,18

Despite the effectiveness of HPV vaccination, a vaccination strategy alone will not benefit large cohorts of older GBM/GDP and those with prior HPV infections.^11,19,20 Furthermore, HPV vaccine effectiveness among GBM vaccinated at older ages is considerably lower as it only protects against new infections, not existing ones.²¹ Screening for and treating high-grade squamous intraepithelial lesions (HSIL)—precancerous growths that precede anal cancer—is an effective compliment to HPV vaccine programs.²² This strategy, mirroring cervical cancer screening protocols, involves initial identification of patients with HSIL using anal cytology. Patients screened positive are referred for high-resolution anoscopy (HRA) to find and treat HSILs—thus preventing anal cancer.²² The International Anal Neoplasia Society (IANS) recommends screening for HSIL among groups with incidence rates >10 times the general population. It is recommended that screening start at age 35 for GBM and transgender women with HIV and 45 for those without HIV.²³ No recommendations were made for other TGD populations.

Even GBM/TGD who are actively engaged in HIV preventive care are not adequately informed about anal cancer, nor are they utilizing anal cancer prevention strategies. For example, individuals prescribed pre-exposure prophylaxis (PrEP), medication to prevent HIV infection, are routinely tested for HIV and other STIs and have regular interactions with healthcare providers. Yet, in a community-based survey of GBM and TGD in the United States, just 43.8% of vaccine eligible PrEP users had initiated HPV vaccination.²⁴ In a separate survey of vaccine-eligible Black and Hispanic GBM and TGD, just 46.5% had initiated HPV vaccination and PrEP use was not associated with greater uptake.²⁵ In a clinic-based review of medical charts, just 21.8% of PrEP patients in a family medicine clinic had received HPV vaccination despite recent and frequent contact with their healthcare providers.²⁶ Finally, in a study of GBM/ TGD accessing PrEP at a federally qualified health center, most were uninformed about anal cancer and wanted more information.²⁷ In addition, most respondents indicated that they would be more likely to initiate HPV vaccination if it was offered during their PrEP management visits. Thus, we propose that promoting HPV vaccination within the PrEP care delivery system will increase the reach of anal cancer prevention for GBM/ TGD. But future intervention studies need an explanatory model to guide implementation strategies.

The Information-Motivation-Behavioral Skills (IMB) model has been successfully used to predict HIV preventive behaviors in GBM.²⁸ Applied to this study, the IMB model will provide a framework for understanding what information is currently used to motivate anal cancer prevention behaviors (eg, HPV vaccination and anal cancer screening) and how the deleterious effects of stigma might impact disclosure and candid discussions about anal cancer risk (behavioral skills). Because anal cancer prevention is largely clinically based, we also used Andersen’s Healthcare Utilization model to identity predisposing (ie, sociocultural factors that influence healthcare utilization), enabling (ie, factors that facilitate utilization), and need-based factors (ie, an individual’s need for specific services). This theoretical approach served as the basis for the data collection and interpretation. We sought to describe the key constructs in relation to anal cancer prevention within the context of PrEP healthcare utilization. To accomplish this, we addressed the following research questions: (RQ1) What information, motivation, and behavioral skills underlie decision making about anal cancer prevention through (a) HPV vaccination and (b) anal cytology screening? (RQ2) How do specific patterns of healthcare utilization among people on PrEP impact their ability and willingness to engage in anal cancer prevention?

Methods

This study employed qualitative in-depth individual interviews.

Participants and Procedures

Purposive sampling was used to recruit PrEP users in the United States based on age, gender identity, and ethnoracial identity. The goal was to facilitate information representativeness from groups that experience anal cancer disparities, underutilize HPV vaccination, and experience intersectional stigma that may underlie decisions around HPV vaccination. PrEP users ranged in age from 18 to 45.

PrEP users were recruited from a variety of sources including: (1) primary healthcare clinics, (2) social media advertisements, and (3) community-based venues. Eligibility requirements for participants included: (1) being eighteen years or older; (2) currently taking PrEP (self-reported); (3) being located within the United States; (4) identifying as part of a sexual or gender minority group; (5) ability to read and speak English. Recruitment materials described the purpose of the study as improving healthcare for people taking PrEP. An online screener questionnaire was used to determine eligibility and provide informed consent. A waiver of documented consent was approved to increase confidentiality. We conducted in-depth, semi-structured interviews with each of the participants. Interviews were conducted virtually via Zoom by 4 trained interviewers and lasted between 30 and 60 min. The interviews were audio recorded and transcribed verbatim. Participants were thanked for their time and offered a $50 Visa gift card.

Interviews began with a verbal acknowledgment that the participant understood the consent document and agreed to be recorded (video was not required). Interview audio was recorded using Zoom. Interviews followed a semi-structured (Appendix A), open-ended format based on key constructs from the IMB model and Anderson’s Model of Healthcare Utlization.^21,29 The interview questions were pilot tested with 3 members from the priority population who provided feedback on the wording and clarity of questions. All procedures, including informed consent, were approved by the Institutional Review Board (Protocol # 30338) at Temple University.

Data Analysis

The audio was transcribed verbatim. Full text transcripts were imported into ATLAS.ti for coding. The analysis was conducted in 3 phases using separate coding cycles.³⁰ First, structural codes were deductively applied using a priori codes developed from the IMB and Andersen’s model. This was a group-based iterative process to ensure that the codebook was complete and that all data analysts consistently applied the codes. All 4 interviewers participated in the coding along with an additional research assistant who did not conduct any interviews. Second, the structural codes were isolated and inductively analyzed using descriptive coding. Third, theoretical coding (ie, relating all subsequent codes to a core concept) was then used to integrate and synthesize all codes into an explanatory model with a constant focus on the utilization of anal cancer prevention services. Consistency and trustworthiness for coding were iteratively established between the PI and the research team. Member checking (ie, gather feedback on the codebook, code definitions, and themes) was established through regular meetings with a community advisory board consisting of individuals from the priority population and a separate advisory board of PrEP providers.

Results

Sample characteristics are reported in Table 1 (N = 36). There was diversity in age (M = 30.6; SD = 6.7) and ethnoracial identities (eg, 42.4% Hispanic; 27.3% non-Hispanic White; 18.2% Black/African American). Most participants identified as cisgender gay men (78.9%) and were college educated (81.8%).

Table 1.

Sample Characteristics (N = 33).

Variable	n (%) or mean (SD)
Age, mean	30.6 (6.7)
Vaccine age group
18-26	12 (36.4)
27-45	20 (60.6)
>45	1 (3.0)
Sex at birth
Male	30 (90.9)
Female	3 (9.1)
Gender identity
Cisgender man	26 (78.8)
Nonbinary	2 (6.1)
Transgender man	2 (6.1)
Transgender woman	3 (9.1)
Sexual identity
Gay	26 (78.8)
Bisexual	1 (3.0)
Pansexual	5 (15.2)
Queer	1 (3.0)
Ethnoracial identity
Non-Hispanic White	9 (27.3)
Non-Hispanic Black	6 (18.2)
Hispanic	14 (42.4)
Asian	1 (3.0)
Multi-racial	3 (9.1)
College educated
Yes	27 (81.8)
No	6 (18.2)
HPV vaccine completion
No	13 (39.4)
Yes	20 (60.6)
Age at HPV vaccine completion, mean	21.8 (6.1)

Descriptive coding identified 29 distinct concepts related to anal cancer prevention that were nested within key constructs from the IBM model and Anderson’s model of healthcare utilization. Each concept and related summary are described in Table 2. Emergent codes included those related to the cultural responsiveness of healthcare received by participants as well as the utilization of telemedicine services (ie, “TelePrEP”). Three interrelated processes were articulated that included individual decision making, established healthcare utilization patterns, and characteristics of the healthcare system.

Table 2.

Qualitative Coding, Summaries, and Representative Quotes (N = 33).

Construct and descriptive codes	Summary	Representative quotes
Information: Knowledge and misinformation	Participants were generally aware of HPV and HPV vaccination, but their knowledge was limited.	“I know that some strands of HPV can cause warts, including like anal warts.” (P015, 18-26, cisgender man, vaccinated) “I’ve heard of HPV as from like getting the vaccine.” (P014, 27-45, cisgender man) “I know that when we learned about it in high school, it was mostly taught to girls and like, we just had to pay attention. And it was mostly a thing that the girls had to pay attention to. Because it can cause cervical cancer.” (P001, 27-45, cisgender man, not vaccinated)
Information: Misinformation	There were misperceptions that HPV was a women’s health issue and only adolescents could be vaccinated.	“I was always confused that . . . the most I know about it [HPV] is . . . that it is a ghost in men’s bodies and goes BOO in women’s bodies.” (P024, 27-45, cisgender man, vaccinated) “Yeah, I asked my doctor. I’ve asked like two different doctors throughout the years, and they both kind of said I was too old for [the HPV vaccine].” (P033, 27-45, cisgender man, not vaccinated) “So what I heard from my friend, and my boyfriend, is that anal cancer in gay men is lower than heterosexual men because . . . they like douche and they feel their prostate and all of that.” (P031, 27-45, cisgender man, not vaccinated) “I just brought it up [anal pap] and the provider that I spoke to . . . she was just kind of like ‘wait, what?’ . . . she was like, ‘I have a pap smear. I get one. You don’t have a vagina. Why would you need one’. . .” (P013, 27-45, cisgender man, vaccinated)
Information: Understanding of Anal Cancer	There was limited knowledge about anal cancer, including almost no awareness of anal cancer risk factors. Anal cancer was also confused with other more common cancers.	“I didn’t know that exist . . . I didn’t know HPV caused anal cancer.” (P009, 27-45, cisgender man) “Is it different than prostate cancer? Well, it must be.” (P024, 27-45, cisgender man, vaccinated)
Information: Awareness of Anal Cancer Screening	There was a lack of awareness of the availability and purpose of anal cytology.	“I’ve heard of the Pap smear, like for like a GYN exam or something? I don;t know exactly what it is.” (P006, 18-26, cisgender man, vaccinated)
Information: Need for proactive communication from healthcare providers	Personal health behaviors like HPV vaccination and regular STI testing. Varied interactions with healthcare providers. Importance of sexual health education highlighted.	“I feel like, it would be nice if the doctor would already just mention these, this type of care or like these screenings, because like, if they already know, like their patients are having anal sex, they should be like, ‘okay, like, when was the last time you had an anal pap smear’ and stuff like that. So, I feel like if they were to bring it up on their own, because they know what type of clients they’re seeing, that would make it a lot more comfortable just having those conversations.” (P014, 27-45, cisgender man) “I’m part of that age range of when HPV shots were being given out to teenage girls. And then at some point, it was available for men. I got mines this year, got my third shot this year . . . I went to speak to my doctor about it, because a really good friend of mines, her ex-boyfriend or something, had somehow contracted HPV . . . And I didn’t even know that I could get the shot. I thought that it was only for women. So, I go to talk to my primary care. And I was like, ‘hey, like, you know, I’m here every three months for my panel testing and to get my prep re-administered. You guys have never mentioned anything to me about being like, have I ever had the vaccine for HPV? And I want to know, like, why?’ And they were like, ‘oh, you know, like, you can get it.’ They didn’t have a why? Like, they didn’t have like a why they didn’t ask me.” (P030, 27-45, cisgender man, vaccinated)
Motivation: Guidance from Healthcare Providers	Many participants highlighted the importance of seeking advice and information from healthcare providers regarding cancer screenings and prevention methods.	“I’m just the type of person that believes and trusts the recommendations of doctors or like any type of vaccine recommendation. So whenever there’s a vaccine offered to me, I usually just say yes like when monkey pox first came on, and I wasn’t at the highest risk for monkey pox. I still got the vaccine.” (P014, 27-45, cisgender man)
Motivation: Sexual risk behavior	Participants were motivated by their own assessment of their sexual risk factors, practically around receptive anal sex.	“Yeah, I mean, I guess if you’re having anal sex, receptive anal sex, you might want to get an anal pap smear if you are concerned about your risk for HPV, causing like cancer.” (P028, 27-45, cisgender man, not vaccinated) “I am more of like 80/20 when it comes to giving versus receiving, so that lowers my risk slightly, but it’s not like I don’t have anal receptive sex, you know, from time to time. But that being said, I hope that between the fact that I don’t do it as often and also that I had the HPV vaccine is something that I don’t have to worry too much about.” (P013, 27-45, cisgender man, vaccinated)
Motivation: Peace of mind	Some emphasized the proactive approach toward health and the sense of security that comes from taking preventive measures against HPV.	“It [HPV vaccination] gives you that sense of comfort of knowing that no matter what my chances are lower than if I didn’t get it.” (P001, 27-45, cisgender man, not vaccinated) “I don’t see any downsides [to vaccination]. If anything, it’s just more like a peace of mind. That’s just one less disease I have to worry about in the future. I feel like now knowing about the Pap smear, it does make me feel a lot more comfortable knowing that there are some steps that I could take to advocate for screening just for my own peace of mind where even if, if anything that could be found is detected earlier that it may be that it won’t lead to any type of fatal consequences.” (P014, 27-45, cisgender man)
Motivation: Prevention mentality	Participants highlighted the value of taking preventive measures toward sexual health that encompasses PrEP, in addition to HPV vaccination and the possibility of anal cancer screening.	“I think general how or just, I guess my opinions about it is just um having fun, but in a responsible way. Yeah, I think that’s just my overall view of it.” (P017, 27-45, cisgender man, not vaccinated) “If I can go get it to prevent it, I’m going to go get it to prevent it.” (P025, 27-45, cisgender man, not vaccinated)
Motivation: Responsibility toward partner’s health	There was a sense of responsibility in protecting the health of sex partners which influenced decisions around prevention behaviors like HPV vaccination and PrEP use.	“It’s for the health and safety of others, because if I have HPV in a way that can cause anal cancer, that gentleman or woman that I’m allowing to penetrate me and then they go on to penetrate other wonderful people are going to potentially pass that on.” (P013, 27-45, cisgender man, vaccinated)
Behavioral Skill: Communication self-efficacy	Many participants exhibit confidence in initiating conversations with healthcare providers about cancer prevention, vaccines, and screenings; however, some are inhibited by stigma around sexual health conversations.	“I think, basically just go with this information and talk to my doctor. . . Should I be getting screened?” (P017, 27-45, cisgender man, not vaccinated) “I would put Dr. [OMITTED] through the gauntlet every time I met with her. I’m pretty open in terms of discussing my health and everything.” (P006, 18-26, cisgender man, vaccinated) “I would ask my doctor about anal cancer prevention and try to integrate it into my healthcare routine.” (P007, 18-26, cisgender man, vaccinated) “I’d initiate the conversation, but I wouldn’t like volunteer any information, I would just sort of answer questions afterwards.” (P003, 27-45, cisgender man, not vaccinated)
Behavioral Skill: Utilization of Digital Tools for Health Information	Participants proposed to use digital tools, including AI platforms like ChatGPT, to gain quick overviews of anal cancer information in order to make informed decisions about HPV vaccination and anal cancer screening.	“The first step I think would be the internet. Making sure that it’s a reputable website, of course. Um, I think that the Mayo Clinic has good information out there. Without giving too much scientific information that it’s very hard to digest or to understand . . . that’s the one that comes to mind. I mean, WebMD comes to mind, but I don’t think that that I would trust that very much.” (P016, 27-45, cisgender man, not vaccinated) “I can just ask ChatGPT, can you explain to me really quickly, I can put in my sort of basic demographic data in a prompt and just be like, okay, like, what’s the relevant information for me, and then it’ll approximate, you know, like, it’ll give an informative sort of overview, I wouldn’t trust it with medical decisions. And it would even probably make that disclaimer, as well. But it’s, it’s just kind of like an easy way to just kind of get a quick overview of something.” (P020, 27-45, cisgender man, vaccinated)
Behavioral Skill: Navigating Healthcare Accessibility Challenges	Some participants discuss the challenges in accessing anal cancer prevention due to changes in policies or lack of provider knowledge.	“In China, HPV vaccinations are only allowed for women . . . after I moved here, I realized that I can use my insurance to go to CVS or Walgreens . . .” (P007, 18-26, cisgender man, vaccinated) “I’ve asked like two different doctors throughout the years, and they both kind of said I was too old for it [HPV vaccination].” (P033, 27-45, cisgender man, not vaccinated)
Predisposing: Intersectional identities and health	The perceived lack of relevant health information for minoritized communities contextualizes interactions with health information and providers.	“Especially as a person of color, I think there isn’t enough information for people who are part of the LGBTQ+ community who are of color.” (P001, 27-45, cisgender man, not vaccinated)
Predisposing: Social Factors	The social environment among LGBTQ peers influence healthcare decisions.	“Everyone, in my friend group was on it [PrEP], essentially.” (P003, 27-45, cisgender man, not vaccinated) “I felt like it [PrEP] was necessary. Just because my boyfriend and I, we recently just became open, and we don’t go out sleeping with everybody, but just to be more safe and more cautious of like what’s out in the environment. And also, the fact that I would say most of all my close guy friends and even some of my girlfriends are on PrEP.” (P031, 27-45, cisgender man, not vaccinated)
Predisposing: Affective Factors	Fears and anxieties about HIV have shaped attitudes toward preventive measures.	“I had multiple, like instances where there were like, a lot of fear and anxiety around HIV.” (P015, 18-26, cisgender man, vaccinated)
Predisposing: Attitudes toward vaccines	Positive attitudes toward vaccines in general.	“I grew up in a very pro-vaccine household. And my parents, my mom especially would just encourage us to, like, protect us by ourselves as much as possible.” (P002, 27-45, cisgender man, not vaccinated)
Predisposing: Risk perceptions	Many individuals mentioned that their sexual behavior, such as having multiple sexual partners or engaging in unprotected sex, influenced their perception of risk.	“I want to know, definitely the risks and things like that just as a gay man who practices both topping and bottoming” (P002, 27-45, cisgender man, not vaccinated) “Everyone is responsible for their own sexual health . . . So, using PrEP for me was, as someone who has multiple partners, and is not necessarily monogamous, it was part of my responsibility . . . to my partners to be responsible, same if I use condoms or any other type of protection.” (P023, 27-45, cisgender man, not vaccinated)
Predisposing: Specialized sexual health care	Individuals who decided to start PrEP often sought specialized clinics or healthcare providers with expertise in sexual health and STI prevention.	“I don’t think I would go to my primary doctor, because . . . I guess, more general, doctors are not too entirely familiar with PrEP.” (P004, 27-45, cisgender man, not vaccinated)
Enabling: Regular Health Checkups	Participants frequently mentioned regular health checkups as a key factor enabling healthcare utilization.	“I went to my primary health care provider beginning of the year . . . yearly checkup and wanted to do an STI panel.” (P002, 27-45, cisgender man, not vaccinated) “I’m here every three months for my panel testing and to get my prep re-administered.” (P030, 27-45, cisgender man, vaccinated)
Enabling: Fragmented healthcare	Some participants selectively fragment their sexual health from their primary care. Many turn to telehealth providers for PrEP.	“It’s just for PrEP. I go to an actual doctor, you know, for my physical every year?” (P021, 27-45, cisgender man, not vaccinated) “I had always gone to like LGBT health centers for PrEP. So, they were like, certainly places that were familiar with working with LGBT people and prescribing PrEP and things like that. And then my current provider is through a clinic that I get as like a benefit through my employer. I was getting prep through a different provider. . . but then I was going to this provider for like, kind of more regular checkups and like, smaller, like, health concerns.” (P015, 27-45, cisgender man, vaccinated)
Enabling: Insurance Coverage	Insurance coverage is crucial for consistent healthcare access. Participants discussed how insurance impacts their ability to receive regular healthcare services, including PrEP and STI testing. Some were able to acquire PrEP for free, but lacked insurance to cover primary care.	“After I moved here, my student insurance wasn’t covering everything. So, I called a health center. They hooked me up with PrEP. Since then, they have given me free medication.” (P007, 18-26, cisgender man, vaccinated) “I was trying to save this cost and but I find weird that here in the US I used insurance so I don’t pay but like the price of if I if I didn’t have insurance, I would have to pay like 3k.” (P019, 27-45, cisgender man, vaccinated) “My health insurance, it’s been on and off for a couple years, now I need to go back, but it’s been like two years [since having a primary care doctor].” (P001, 27-45, cisgender man, not vaccinated)
Enabling: Relationship with Healthcare Provider	A good relationship with healthcare providers, characterized by trust and understanding, especially in the context of LGBTQ+ health, significantly influences healthcare utilization.	“My sexual health doctor, she’s really cool. So, you know, she’s always awesome. She talks to me about other things other than my sexual health, so I appreciate that about her. So it’s always been a positive energy there.” (P008, 18-26, cisgender man, not vaccinated) “But I never felt like judged or, or I never feel judged by her like, she listens, she provides the health recommendations that she has true and etc.” (P019, 27-45, cisgender man, vaccinated)
Enabling: Availability of LGBTQ+-affirmative providers	Availability of LGBTQ+-friendly healthcare services, including those knowledgeable about PrEP and sexual health, is key to enabling healthcare utilization for many participants.	“They’re focused on like, health care for people with HIV, they have like, a strong involvement with the LGBTQ community.” (P006, 18-26, cisgender man, vaccinated)
Enabling: Access to telehealth	Telehealth services facilitate healthcare access, especially for PrEP and STI testing.	“It’s an online health service . . . They send you a kit via mail, where you do all your testing . . . then you have a virtual conversation with a doctor.” (P001, 27-45, cisgender man, not vaccinated) “Twice a year, I have to have like a Zoom meeting with the doctor.” (P033, 27-45, cisgender man, not vaccinated)
Need: Sexual Behaviors (eg, anal sex, number of partners)	Many participants acknowledged engaging in sexual behaviors that increase anal cancer risk. The level of sexual activity varied, with some having multiple partners and others being more cautious.	“I felt like it was necessary. Just because my boyfriend and I, we recently just became open, and we’re very we don’t go out sleeping with everybody and anyone, but just to be more safe and more cautious of like what’s out in the environment.” (P031, 27-45, cisgender man, not vaccinated) “I consider myself like, a verse-bottom. I do bottom pretty often. I feel like my chances of maybe getting, anal cancer or any other type of diseases in the future might be a lot higher than anyone who doesn’t participate in anal sex.” (P014, 27-45, cisgender man) “I started becoming more open to the idea of like unprotected anal sex.” (P006, 18-26, cisgender man, vaccinated)
Need: STI History and Health Concerns	A history of STIs and other health issues influenced participants’ assessment of their risk. There is a sense of acceptance of increased risk for STIs and an equal sense of diligence in testing and treatment.	“I mean, now that you mentioned it, I probably might have mistaken in getting the HPV vaccination. So that’s something I would definitely look into getting now, due to the risk. Because I was told I was recently diagnosed with sickle cell. So I’m just sure that also might, you know, increase the risk for me.” (P008, 18-26, cisgender man, not vaccinated) “I had like a really bad bout of like internal herpes.” (P010, 27-45, transgender/non-binary, not vaccinated) “I had monkey pox in October.” (P006, 18-26, cisgender man, vaccinated) “I had been traveling, went to a gay vacation destination over the summer, went to a couple of different parties and had sex with some really awesome men had sex with some really awesome trans people. And did get a wonderful text message of hey, you know, so and so tested positive for syphilis. So everybody who was at the party should just go and get checked out. So I you know, kind of did the math Okay, am I within the window, am I here? So I waited a couple of days and then went got checked out just because it was easy as a walk in versus going to my doc where you know, appointments, scheduling, so on and so forth.” (P013, 27-45, cisgender man, vaccinated)
Cultural Responsiveness: Awareness and Sensitivity to LGBTQ+ Health Needs	Participants’ experiences with healthcare providers varied significantly. Some felt their sexual orientation and specific health needs were neglected or misunderstood, while others reported more positive interactions with culturally competent providers. A recurring theme was the need for providers to be non-judgmental and knowledgeable about LGBTQ+ specific health risks, such as HPV and HIV.	“I don’t think that there is enough of an intentionality behind asking people if you are part of the LGBTQ+ community. I choose a doctor’s kind of like choosing a therapist, like when I choose a therapist, I want someone who understands my culture.” (P001, 27-45, cisgender man, not vaccinated) “And I found out that not every doctor was familiar with it with PrEP, or what it did. So, they had to find out more information . . . But my impression from that meeting is that he had no idea what I was talking about. So yeah, I mean, like, I want to believe that he didn’t know he probably just either forgot or he was uncertain or whatever reason. But to me, but it wasn’t the first time that I’ve come across some doctors who, you know, they’re not prejudiced or anything like that. They just didn’t seem to really have heard of it.” (P033, 27-45, cisgender man, not vaccinated) “I didn’t really have a primary care. Um, I think there’s a lot of gender dysphoria mixed in there, being treated a certain way at offices, less inclusivity. Ever since I’ve started going to [omitted] . . . they just are really considerate and make me feel very comfortable. It’s very inclusive. It’s a very positive experience that I had never experienced before. I didn’t know going to the doctor could be so positive.” (P010, 27-45, transgender/non-binary, not vaccinated) “It was a rocky start to begin with, because my general primary doctor, when I started to become sexually active. He was very confused, because I was probably like, 19. At that time, he was very, I guess I could say, old school. He was very confused. Like, he was my family doctor. And he was very confused, like, ‘Well, why do you want to get tested for this?’ I felt very judged, in a way, I guess you can say. So I had to change. I had to change a primary because I just felt like he was uncomfortable.” (P011, 27-45, cisgender man, not vaccinated)
Telemedicine: Barrier to comprehensive care	Many participants utilized telehealth services for PrEP because of cost, convenience, and lack of interaction. This may be done in addition to or instead of primary care.	“It goes into your house, which I think it’s super nice that you could be that could be much more accessible to people.” (P029, 27-45, cisgender man, vaccinated) “I think it’s because there is limited interaction, and I just get what I need [i.e., PrEP].” (P001, 27-45, cisgender man, not vaccinated) “They asked you if you have insurance . . . but I know they still provide it [PrEP] to you even without insurance.” (P004, 27-45, cisgender man, not vaccinated) “Twice a year, I have to have like a Zoom meeting with the doctor.” (P033, 27-45, cisgender man, not vaccinated) “I think the information is more secure, I really don’t want my personal doctor, knowing, you know, all my information.” (P021, 27-45, cisgender man, not vaccinated)

Individual Decision Making

The synthesis of findings using the IMB model highlighted key aspects influencing anal cancer prevention behaviors. While participants exhibited a baseline level of information (eg, HPV can cause anogenital warts and cervical cancer), misinformation (eg, HPV is worse for women), and knowledge gaps (eg, lack of awareness of anal cancer risk factors) were present. For example, one participant highlighted the lack of information about the direct health consequences of HPV in males: “. . . the most I know about it [HPV] is . . . that it is a ghost in men’s bodies and goes BOO in women’s bodies.”

There was nearly no awareness of anal cancer screening modalities (eg, anal cytology). When information gaps were addressed in the interview, participants exhibited a high degree of motivation to engage in preventive measures; however, they reiterated the importance of healthcare providers in making these decisions. Other motivators were their own perceptions of their sexual risk behaviors, which were managed with harm reduction strategies (eg, routine STI testing). The following quote highlights the individual risk assessments done based on anal sex behavior: “Yeah, I mean, I guess if you’re having anal sex, receptive anal sex, you might want to get an anal pap smear if you are concerned about your risk for HPV, causing like cancer.”

However, the actual engagement in anal cancer preventive behaviors is likely contingent upon participants’ behavioral skills, including their ability to initiate conversations about their sexual health with healthcare providers, advocate for themselves, find reliable health information using web-based tools, and navigate the healthcare system. Some were very proactive about their health, “I would put [doctor] through the gauntlet every time I met with her. I’m open in terms of discussing my health and everything,” while others were more withholding: “I’d initiate the conversation [about anal cancer prevention], but I wouldn’t like volunteer any information. I would just sort of answer questions afterwards.”

Healthcare Utilization

All participants were actively engaged in healthcare that was primarily focused on HIV prevention using PrEP. HIV/STI testing was a part of this focus. The synthesis of findings through Anderson’s model of healthcare utilization revealed that the driving force toward healthcare utilization was an individual’s evaluation of their need for PrEP stemming from their sexual behaviors (ie, receptive anal intercourse, number of partners), relationship contexts (eg, nonmonogamy), fears of becoming infected with HIV, and motivations from previous STI infections. Even among men in relationships, there is a need to assess risk: “I felt like it [PrEP] was necessary. Just because my boyfriend and I, we recently just became open, and we’re very . . . we don’t go out sleeping with everybody, but just to be more safe and more cautious of like what’s out in the environment.”

Participants were regularly seeing healthcare providers within the PrEP context, which enabled them to receive sexual healthcare, but was limiting in important ways. For some, healthcare was fragmented into PrEP care and primary care: “I had always gone to like LGBT health centers for PrEP. So, they were like, certainly places that were familiar with working with LGBT people and prescribing PrEP and things like that. And then my current provider is through a clinic that I get as like a benefit through my employer. I was getting prep through a different provider . . . but then I was going to this provider for like, kind of more regular checkups and like, smaller, like, health concerns.”

The fragmentation of PrEP care from primary care was facilitated by the availability of targeted telehealth services (ie, TelePrEP), which increased the accessibility of PrEP: “It’s an online health service . . . They send you a kit via mail, where you do all your testing . . . then you have a virtual conversation with a doctor.” For some these services increased their access to sexual health services by offering PrEP and related HIV/STI testing at no cost. But there was a disconned for some between their telemedicine PrEP provider and their primary care provider (if they had one): “I think the information is more secure, I really don’t want my personal doctor, knowing, you know, all my information.”

But having good relationships with LGBTQ+ affirming providers was essential in maintaining engagement with care. As one participant described, “I don’t think that there is enough of an intentionality behind asking people if you are part of the LGBTQ+ community. I choose a doctor’s kind of like choosing a therapist, like when I choose a therapist, I want someone who understands my culture.”

In general, the participants in this study had positive attitudes toward vaccines and had social networks that normalized sexual healthcare. Risk perceptions for HIV and related anxieties were motivating factors. Intersecting identities and a perceived lack of personalized care was a motivation for some to seek specialized services at specialized sexual health clinics, TelePrEP, or with specific providers known to be LGBTQ+ affirming.

Healthcare System

The healthcare system’s responsiveness (or lack of responsiveness) to LGBTQ+ health needs emerged as a critical theme, with varying experiences reported by participants. While some praised the availability of LGBTQ+ affirmative services and/or the benefits of telemedicine for accessing PrEP, others recounted experiences of cultural insensitivity: “I didn’t really have a primary care [doctor]. Um, I think there’s a lot of gender dysphoria mixed in there, being treated a certain way at offices, less inclusivity.” Many participants utilized telehealth services for PrEP because of cost, convenience, and lack of interaction (ie, driven by anticipated stigma). This was done in addition to, or instead of, primary care. For many of these participates, anal cancer prevention services would require them to seek care outside of their current PrEP care context (eg, go to a local provider for vaccination and/or screening).

Explanatory Model

Figure 1 presents a conceptual model integrating 3 key processes related to anal cancer prevention (see Table 2 for a complete summary of individual codes): individual decision-making, healthcare utilization, and the healthcare system. Individual decision-making is guided by the IMB model, with information (eg, anal cancer knowledge, HPV misinformation), motivation (eg, prevention mentality, sexual risk behaviors), and behavioral skills (eg, navigating healthcare systems, communication self-efficacy) shaping actions. Healthcare utilization is influenced by predisposing factors (eg, intersectional identities, risk perceptions), enabling factors (eg, access to LGBTQ+-affirming providers, telehealth), and needs (eg, STI history, sexual behavior). The healthcare system includes facilitators like LGBT-affirming environments and telemedicine, but barriers such as HPV misinformation and fragmented care persist. Ultimately, the model highlights that access to culturally responsive care and proactive use of health information tools are critical to improving anal cancer prevention for SGM individuals.

Figure 1.

Explanatory model of anal cancer prevention utilization.

Discussion

The findings of this study demonstrate unmet needs for accurate and targeted anal cancer information among PrEP users. There were significant knowledge gaps and misconceptions about anal cancer and HPV, highlighting the necessity for improved patient education and targeted messaging. Additionally, there were important barriers within the healthcare system that impeded the utilization of existing and future anal cancer prevention services (eg, HPV vaccination, screening) and underscores the importance of culturally responsive care.

Anal cancer prevention is nearly absent from ongoing efforts to promote HPV vaccination. High-risk populations, including GBM who have received HPV vaccination, remain largely unaware of anal cancer.⁵ This disconnect may stem from the original marketing of HPV vaccination as a cervical cancer prevention measure, framing it as a women’s health issue.³¹ This history continues to influence perceptions of HPV, as reflected in this and other studies.^7,32 However, the stigma associated with anal cancer cannot be overlooked. Stigmas related to the body (ie, the anus), sexual behaviors (ie, receptive anal intercourse), and marginalized identities (ie, sexual and gender minorities) further complicate discussions and awareness of anal cancer prevention.³³ To overcome these barriers, targeted campaigns—similar to those used to promote PrEP—are needed to increase awareness and destigmatize anal cancer prevention discussions.³⁴

PrEP providers play a crucial role in counseling patients about anal cancer risks and prevention. As our findings indicate and previous studies have found, patients may be uncomfortable initiating conversations about receptive anal intercourse.³² To address this, providers should proactively address misinformation about HPV (eg, it’s not solely a women’s health issue), risks associated with receptive anal intercourse, and prevention through HPV vaccination (eg, it’s not only for adolescents). Providers should also discuss anal cancer screening with populations for which anal cytology is recommended.^35,36 Employing sex-positive messages that highlight the benefits of anal cancer prevention, beyond just cancer prevention, may resonate more with this population.

For many GBM and TGD populations, sexual healthcare is the primary motivator for healthcare utilization, driven by the need to mitigate HIV risk and protect sexual health.^37
-39 PrEP users, motivated by these concerns, are potentially early adopters of anal cancer prevention services like HPV vaccination and anal cancer screening. However, their interactions with the healthcare system, primarily focused on PrEP adherence and routine STI testing, act as barriers.²⁷ Given that PrEP management visits often constitute the only healthcare interactions for many young and healthy GBM/TGD populations, these touchpoints and patient-provider relationships should be leveraged to integrate comprehensive, equitable, healthcare.²⁷ However, PrEP can be highly specialized, often guided by internal electronic medical record templates, which may not address broader healthcare needs.²⁷ Ensuring that PrEP patients’ primary care needs are met is essential for providing equitable care.

While telemedicine increases access to PrEP, it may also limit comprehensive care due to reduced interactions and niche service delivery. Opportunistic or unscheduled vaccinations can occur during various clinical visits, including sick visits, unscheduled STI testing, or chronic illness management.⁴⁰ The use of standing order protocols—pre-authorizing nonphysician healthcare professionals to assess and administer vaccines—is effective and recommended by the Advisory Committee on Immunization Practices.^41,42 However, implementing these protocols is complicated by telemedicine’s limitations, requiring additional steps from patients (eg, schedule vaccination at a local pharmacy). Most PrEP users receiving care via telemedicine complete their appointments and required lab testing remotely, eliminating opportunities for vaccination. More research is needed to identify ways to connect telemedicine PrEP users to local LGBTQ+-affirming healthcare services.

Our explanatory model integrates theoretical approaches from the IMB and Anderson’s models to highlight key barriers and facilitators to anal cancer prevention among PrEP users.²¹ The proposed model underscores the importance of accurate information, patient motivation, and behavioral skills in individual decision-making about anal cancer prevention. Additionally, it emphasizes the role of healthcare utilization patterns and the responsiveness of the healthcare system in shaping anal cancer prevention behaviors. By addressing misinformation, enhancing healthcare provider-patient education, and ensuring access to LGBTQ-affirmative comprehensive care, the model provides a framework for developing effective intervention strategies.

This in-depth qualitative study has several limitations. The use of purposive sampling, while valuable for ensuring diverse representation, may limit the generalizability of the findings. As noted, most participants identified as cisgender males. More research is needed to identify the needs of transgender women and other TGD populations. As we focused on individuals already engaged in PrEP care, these perspectives may not be representative of those less connected to healthcare services. As with other self-report studies, introduced recall bias and social desirability bias may have influenced responses to the interview questions. Additionally, the virtual nature of the interviews might have influenced the depth and dynamics of the interactions. Because of the exploratory nature of this qualitative study, the results should be considered preliminary and hypothesis-generating. Despite these limitations, the findings provide rich and nuanced insights into barriers and facilitators of anal cancer prevention among a diverse group of PrEP users.

This study highlights the urgent need to integrate anal cancer prevention with HIV prevention efforts and STI screening within PrEP care. Policy measures could include requiring local health service contacts for patients receiving PrEP via telemedicine. Targeted messaging should connect anal cancer prevention with sexual risk behaviors like receptive anal sex. Addressing knowledge gaps, enhancing healthcare provider communication, and improving access to LGBTQ-affirmative services are crucial. By leveraging PrEP management visits and telemedicine, healthcare providers can more effectively promote anal cancer prevention. Collaborative efforts among healthcare providers, policymakers, and researchers are essential to reduce anal cancer disparities among at-risk sexual and gender minority populations.

Footnotes

Appendix A

Correction (December 2024):

Since the original online publication, the incorrect Figure 1 has been replaced with the correct one.

Author Contributions

CW and SB contributed to the study conception and design, material preparation and data collection. Data collection was assisted by CF, IWS, CL, and KS. Data analyses were performed by CW, CF, IWS, and CL. All authors assisted with validation of the qualitative findings and interpretation of findings. The first draft of the manuscript was written by CW, and all authors commented on several versions of the manuscript. All authors read and approved the final manuscript.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Research reported in this publication was supported by the National Institute of Minority Health and health Disparities of the National Institutes of Health under Award Number R21 MD017661. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Ethical Considerations

All study protocols were approved by the Temple University Institutional Review Board. Participants received informed consent and gave verbal consent. A waiver of documented consent was approved by the IRB.

ORCID iD

Christopher W. Wheldon

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Needs and Opportunities for Anal Cancer Prevention in Patients Engaged With PrEP Care: Development of Conceptual Model

Abstract

Introduction:

Methods:

Results:

Conclusions:

Keywords

Introduction

Methods

Participants and Procedures

Data Analysis

Results

Individual Decision Making

Healthcare Utilization

Healthcare System

Explanatory Model

Discussion

Footnotes

Appendix A

Correction (December 2024):

Author Contributions

Declaration of Conflicting Interests

Funding

Ethical Considerations

ORCID iD

References