Abstract
Despite being a promising prevention strategy for populations at risk for HIV acquisition, there has not been rapid uptake of HIV antiretroviral pre-exposure prophylaxis (PrEP). Yet, HIV clinics within the Mount Sinai Health System in New York City have successfully incorporated PrEP. HIV care providers (n = 18), who practice in these clinics and were early PrEP adopters, participated in a survey and semistructured interview. Qualitative thematic analysis revealed that barriers and facilitators to PrEP uptake were identified on multiple levels from broader systemic to provider-and-patient-level concerns. The following themes were identified: (1) to reach a greater proportion of patients at risk for HIV and address racial/ethnic and gender disparities, PrEP should be available in a variety of settings and provided by different types of providers within proximity to affected populations; (2) financial support is needed beyond addressing medication cost; and (3) multidisciplinary teams and population-specific clinic protocols can assist providers in conducting high-quality visits and addressing these barriers to PrEP.
Introduction
HIV infection rates remain high with ∼40,000 new cases in the United States in 2018 and an alarming proportion of new infections occurring among black and Hispanic/Latinx populations. 1 Antiretroviral pre-exposure prophylaxis (PrEP) is a promising HIV prevention strategy for patients at increased risk for HIV infection. 2 Approved by the Food and Drug Administration in 2012, emtricitabine/tenofovir disproxil fumarate (Truvada) was the first drug recommended for use as PrEP followed by emtricitabine/tenofovir alafenamide (Descovy) in 2019. 3 –5 Despite proven efficacy and incorporation into clinical guidelines, there has not been rapid wide-scale utilization of PrEP. 1,6,7 A 2018 study by the Centers for Disease Control and Prevention (CDC) found that only a small percentage of Americans who could benefit from PrEP had been prescribed the medication. 8 Similarly, surveys of US primary care providers (PCPs) and HIV specialists indicated high awareness of the efficacy of PrEP but low rates of prescriptions. 2,9,10
Given the slow uptake of PrEP, identifying and addressing barriers to access are crucial. Some acknowledged barriers include insufficient screening, limited time for counseling, inadequate financial coverage, limited adherence, and irregular follow-up appointments. 9,11 Further, provider concerns about unintended consequences prevent many from prescribing PrEP. These concerns include exposing healthy individuals to medication-related toxicities, fears that widespread use will disseminate drug-resistant viral strains, and risk compensation, namely that PrEP users will increase high-risk behaviors based on their reduced risk of HIV acquisition. 9,11 –18
A major challenge in disseminating PrEP is identifying the types of physicians and clinical settings (e.g., HIV clinics, urgent care, or primary care clinics) where the medication should be provided. Although it is seemingly logical for PCPs to screen and provide PrEP as they see primarily HIV-negative patients who may be potentially at risk for HIV acquisition, some PCPs express concern about the screening, counseling, and monitoring required for PrEP. 11 Meanwhile, HIV providers who are experienced in risk counseling and providing antiretrovirals do not routinely care for HIV-negative patients. This contradiction between comfort with providing PrEP and the type of providers who are best positioned to screen HIV-negative populations who are at an increased risk for HIV acquisition is known as the “purview paradox.” 11
To better understand the experiences of HIV and infectious disease (ID) trained providers who were early adopters of PrEP provision, we conducted a qualitative study with a sample of HIV practitioners in New York City. HIV and ID trained providers who were successful early adopters of PrEP provision in a diverse urban setting are uniquely positioned to recognize and successfully address PrEP access inequities within our health care system.
Methods
This study was conducted at the Institute for Advanced Medicine (IAM), a six-site network of hospital- and community-based clinics within the Mount Sinai Health System (MSHS), organized to provide comprehensive care for patients living with HIV and AIDS in New York City. MSHS is an eight-hospital integrated delivery network with >3,499,000 outpatient visits from patients in New York City and surrounding environs. 19 As a clinic network within MSHS, IAM serves >13,000 patients with and at-risk for HIV/AIDS. Clinical services are supported by ∼$12 million in grant-funded programming. 20 In 2014, IAM practices began providing PrEP, and in 2016, it received a grant from the New York State Department of Health's AIDS Institute to expand its PrEP program.
From March through May 2018, internal medicine trained HIV and ID providers were surveyed and interviewed. All clinical providers (physicians, including fellows and nurse practitioners) working within IAM practices were eligible for the study. Forty-six eligible study participants were invited through e-mail. If an eligible provider indicated interest, one of the coinvestigators contacted them to schedule an interview. Providers were selected through a convenience sample where participants were interviewed sequentially in the order in which they responded to the recruitment e-mail. Thematic saturation was reached when a total of 18 providers were interviewed with representation from all IAM clinics. The remaining 28 providers either declined to participate in the study, encountered scheduling issues that prevented their participation before reaching thematic saturation, or did not respond to the recruitment e-mail.
The survey and interview guides were developed by study staff (T.C.K., B.B., and S.S.) and were reviewed by content experts. Topics in the interview guide included discussion of experiences providing PrEP, the appropriateness of providing PrEP in the setting of an ID/HIV clinic, and barriers and best practices for PrEP prescribing, particularly for hard-to-reach populations. Semistructured in-person interviews that lasted from 25 to 60 min were conducted with each participant as well as a 10-min survey that focused on demographics and PrEP prescribing behaviors. Study participants met individually with a member of the research staff to complete both the interview and survey. Written informed consent was obtained from all study participants. Interviews were audio recorded with permission and transcribed verbatim.
From May 2018 through January 2019, we utilized content analysis techniques with an inductive thematic approach to analyze the data. 21 Two members of the research team coded text and developed descriptive themes (T.C.K. and B.B.). These descriptive themes were identified and organized into larger analytical themes. The study team (T.C.K., B.B., and S.S.) then reviewed each analytical theme for internal consistency and any discrepancies were resolved through consensus. The interviews were coded and analyzed using QSR International's NVivo 12. All study procedures were approved by the Icahn School of Medicine at Mount Sinai IRB.
Results
Our analysis reaffirmed that barriers to PrEP uptake exist in societal, provider-focused, and patient-related realms, as has been outlined in previous studies. This study also showed that barriers to PrEP uptake can be addressed through clinic protocols that realign and strengthen resources with a focus on the coordinated use of multidisciplinary teams and targeted financial supports. 22 We found three major themes: (1) to reach a greater proportion of patients at risk for HIV and address racial/ethnic and gender disparities, PrEP should be available in a variety of settings and provided by different types of providers within proximity to affected populations; (2) financial support is needed beyond addressing medication cost; (3) multidisciplinary teams (including nurse practitioners) and population-specific clinic protocols can assist providers in conducting high-quality visits and addressing barriers to PrEP provision.
Our analytic sample included 18 out of 46 eligible providers. The majority of providers were between 30 and 49 years of age (61%), female (61%), physicians (67%), and have been in practice for >10 years (61%) (Table 1). A notable proportion (39%) of the providers identified as a race other than white with 22% identifying as Hispanic/Latino. Notably, the nonphysician providers were nurse practitioners (Table 1). Many (44%) of the providers indicated that they had larger PrEP practices with 50 or more patients (Table 1).
Participant Demographics
Systemic-level barriers and solutions
One of the most commonly reported systems-related problems was insurance coverage. Insurance issues were generally related to lack of coverage of routine testing, such as sexually transmitted infections (STI) testing, and follow-up visits, rather than inadequate medication coverage (Table 2). One provider expressed frustration about a patient who had STI testing done at another clinic to save money, leading to difficulty coordinating care (Table 2). However, one benefit of being able to provide PrEP at an HIV/ID clinic was the potential for grant funding. Some of the IAM clinics were able to provide additional financial support for patients with inadequate insurance coverage (Table 2). The HIV clinics also offered multidisciplinary services that addressed financial or psychosocial barriers to care, such as exploring additional options for financial support. These specialists, nurses, social workers, and care coordinators were also accustomed to providing care to patients with multiple health service needs. One provider observed, “We have social workers and if they need psychiatric help, we refer them to psychiatry” (Participant 9, physician).
Illustrative Quotations That Demonstrate Systemic Barriers and Solutions
ID, infectious disease; nPEP, nonoccupational postexposure prophylaxis; PEP, postexposure prophylaxis; PrEP, pre-exposure prophylaxis.
Another systemic issue is the overall lack of time built into provider schedules to adequately counsel and see more PrEP patients. This meant that there was an emphasis on other staff providing services, so patients would receive adequate counseling and education. These HIV clinic staff members, including nonclinical staff, were well trained and comfortable with providing appropriate harm reduction counseling to patients, which relieved time pressures on clinical providers.
Further, a larger societal issue identified in this study was stigma related to being on PrEP and going to an HIV/ID clinic regularly. One provider described a belief in the community that people on PrEP are promiscuous and, therefore, not interested in self-care: “The perception was that people taking Truvada were highly promiscuous so there was that whole, you know, I am not taking care of myself” (Participant 17, physician). Some providers reported that it was difficult for some patients to go to a clearly identified HIV clinic: “I have a number of patients who really would like to come at a time when people that they know can't see them in this area or at the clinic. So yes, there is still a stigma that still prevails for patients who are HIV-negative who want PrEP, they would probably prefer to go to a regular clinic over an HIV clinic” (Participant 18, nurse practitioner). However, other clinicians who were interviewed stated that the clinics where they practiced had, within the past 5 years, been rebranded and renamed as neighborhood/community-based clinics, rather than HIV-specific clinics. This rebranding made their patients feel more comfortable and reflected a more inclusive approach toward caring for the surrounding community (Table 2).
A major systemic concern highlighted in the purview paradox is the belief that some HIV/ID providers would not be able to provide PrEP due to their belief that providing care for non-HIV patients would be out of their scope of practice. However, we found that most of the providers felt that it was appropriate for ID and HIV providers to prescribe and monitor PrEP and that it was easy to incorporate into the existing clinic model. Some of the providers noted that within the HIV/ID clinics, an important population to screen was patients seeking nonoccupational postexposure prophylaxis (nPEP). Although not all nPEP patients were interested in or appropriate for PrEP, providers found that it was a targeted way to provide screening for PrEP among a subset of patients potentially at risk for HIV and may be more likely to be referred to HIV/ID clinics. For example, as one provider stated, “The bulk of my PrEP patients are referrals from urgent care centers who usually go to the urgent care centers for PEP and who are then referred to me for follow up of PEP and end up being on PrEP” (Participant 11, nurse practitioner). Another provider noted that having a dedicated provider in the clinic who focused on nPEP made it easy for that provider to also screen for appropriateness of PrEP (Table 2). By streamlining a process, including identifying potential nPEP patients and using specifically identified and trained providers, some of the clinics were better able to focus PrEP recruitment efforts on populations more likely to be at an increased risk for HIV acquisition.
Another major systemic concern is the need to diversify the population that is receiving PrEP, given the demographics of those who are most at risk of HIV acquisition. One of the major populations with a high burden of HIV incidence are black and Latino men who have sex with men (MSM), a potentially challenging patient population to reach. 1 Indeed, many of our interviewed providers noted that a majority of their PrEP patients were young black and Latino MSM. They also found that the racial and ethnic mix of their PrEP population was reflective of the neighborhood in which they practiced, indicating that proximity of providers to target populations is crucial. Providers shared that some patients became aware of PrEP through their social and geographic networks: “Word of mouth, like people bring their friends [in for PrEP] a lot” (Participant 4, physician). For these patients, an HIV or community-focused clinic may be a trusted space for PrEP.
Although successful in reaching some groups identified to be at higher risk of HIV acquisition, our providers recognized the need to increase PrEP access for populations with particularly low PrEP uptake, particularly women. Given these recruitment challenges, all providers felt that PrEP should continue to be prescribed both inside and outside of the HIV/ID setting, particularly in primary care. Although incorporating PrEP into the HIV clinic setting was fairly seamless due to provider familiarity with HIV antiretrovirals and the recruitment of HIV-negative patients through nPEP protocols, it was recognized that offering PrEP in additional settings would increase the likelihood that the medication would reach more target populations. As a way to facilitate PrEP provision by other types of providers, many of the interviewed providers recommended the provision of more training to other physicians, which they felt HIV and ID physicians could assist in providing. Some thought that training particular types of providers could support targeted patient outreach efforts. For example, since there is a gender disparity with fewer women on PrEP, training more gynecologists to screen and even provide PrEP could help promote use in a difficult-to-reach population: “I think a gynecologist interfacing with someone who is newly diagnosed with chlamydia is in a position to say, ‘You acquired chlamydia, let's talk about who your partners are and what kind of risk you are at’ and maybe they're not comfortable prescribing PrEP, but it's certainly a good way to link patients to a PrEP provider” (Participant 8, nurse practitioner). Another suggested way to promote PrEP in other clinical settings was for HIV providers to not only provide training, but to also serve as a resource: “I think we do have a role in educating other providers and being there for questions” (Participant 8, nurse practitioner).
Provider-based barriers and solutions
Some providers reported that patients experienced difficulty obtaining PrEP because of other providers or physicians. For example, some noted that patients had come to their clinic seeking more experienced clinicians comfortable with discussing behaviors that may make them at risk for HIV acquisition: “I feel like I get a lot of patients who come in saying their primary care doesn't really take care of that part of it, so they come to see me” (Participant 7, nurse practitioner). Some providers also found that patients were referred to their clinic for PrEP, despite having gone initially to a health care provider who could have potentially prescribed PrEP in their own office (Table 3). A few providers also found that some generalists were not only uncomfortable with but were also improperly prescribing PrEP: “There are a lot people out there who are not using PrEP properly, or whoever is giving them that PrEP, whatever provider, is not doing the right education” (Participant 5, physician). The participants in this study felt it was important to work to counter any stigmatizing and isolating interactions that their patients may have had with other health care providers in the past. The HIV care providers interviewed shared that trained staff who were accustomed to having conversations about sensitive topics and discussing patient concerns made it possible for patients who had previously had negative experiences to reconsider taking PrEP (Table 3). 23
Illustrative Quotations That Demonstrate Provider- and Patient-Level Barriers and Solutions to Prescribing Pre-Exposure Prophylaxis
Patient-level access barriers and solutions
The most widely reported patient-level barrier was adherence to follow-up visits. This issue was thought to be due to multiple reasons including limited availability of appointments, medication that was not used as prescribed, and limited insurance coverage for follow-up appointments and testing. Consistent with CDC recommendations, all clinicians asked PrEP patients to follow-up at least every 3 months. Yet, some felt that the guidelines were too strict and that it would be reasonable to conduct more infrequent follow-ups. Some proposed that visit frequency for patients with consistent risk factors and reliable clinic attendance could be reduced. As one provider described, “I think some patients are really good at using condoms and being on PrEP and know their relative risk factors. It's too rigid to ask people to come back every 3–6 months” (Participant 3, physician). Providers suggested different follow-up models that could facilitate access (Table 3).
Some providers reported that they had patients who deviated from their prescribed or preferred regimen by taking it only when engaging in risky behavior, which often led to infrequent follow-up visits. One provider found that patients needed counseling on ways that PrEP might be rendered less effective, “[I tell patients] not to take it just for the weekends or 5 days of the week, because some people do that, they go to a party and pop a Truvada or share it with friends” (Participant 5, physician). Appropriate and routine medication use counseling was an important component of successfully providing PrEP (Table 3).
Discussion
The goal of this study was to provide insight into the benefits and challenges of providing PrEP within the multidisciplinary HIV clinic model. By focusing on HIV care providers who were early PrEP adopters and their role in the implementation of PrEP, we have highlighted the ability of well-trained and experienced providers and staff to overcome common barriers to PrEP and successfully integrate PrEP into a multidisciplinary outpatient clinic model. Notably, these providers have been able to provide PrEP to black and Latino MSM, a difficult-to-reach population, due to their proximity to these communities and practice in HIV/community clinics that are viewed as trusted and safe places to receive care. We found that the HIV clinics' multidisciplinary team approach allowed providers to utilize support structures and resources to address many of the common challenges to expanding PrEP prescribing.
Although the purview paradox postulates that some HIV clinicians may regard PrEP provision as beyond their scope of duties given their focus on people living with HIV, our study suggests that HIV clinics are able to become ideal settings for PrEP, particularly for patients with complex challenges who need to be cared for by more experienced providers and support staff. This reinforces the need to provide PrEP in multiple clinical settings, including HIV and ID clinics. HIV clinics were able to rebrand themselves to address concerns around stigma and provide care that specifically addresses stigma around use of PrEP. In addition, streamlining clinic structures to identify providers (e.g., those who commonly focus on nPEP or STI screening) to provide PrEP lends itself to successful incorporation of PrEP into the overall HIV/ID clinic model. We found that identifying and training specific staff members allow for high-quality patient care, focused guidance, and the development of PrEP-specific protocols, a model that can be adapted to other settings, as well as other HIV clinics.
There are known challenges around financial support and follow-up for PrEP, regardless of the clinic setting. The providers in this study explained that some of the HIV clinics were able to provide grant funding for financial gaps that extended beyond the direct cost of medication, such as costs related to follow-up visits and routine testing. This suggests that financial support needs to be expanded to address costs other than direct medication costs. In addition, these clinics were able to provide enhanced care through appropriately trained staff, such as social workers and nurses who provided counseling and other supportive services. The support staff allowed for improved scheduling and alleviated the time limitations that other providers may face when trying to incorporate PrEP provision into their demanding clinic schedule. This team-based approach may be incorporated into other existing interdisciplinary models, such as the Patient-Centered Medical Home in primary care, to provide better support for PrEP.
Although it is important for PrEP to be incorporated into the primary care setting, these findings support the idea that PrEP will need to be provided in a wide variety of settings to reach all target populations. Although PCPs should be incorporating PrEP into their practices, HIV clinics will remain important as a source of PrEP prescription/service provision for some communities, for providing support to clinicians who need additional guidance, and in acting as referral sites for cases that are complex. This study found that the patient populations reflected the demographics of the surrounding neighborhood of each clinic, so this study included providers who worked with populations that are traditionally harder to reach such as black and Latino MSM. To reach the racial, ethnic, and gender minorities who experience a disproportionately high burden of HIV incidence, it may be beneficial for policies and grant funding to support community clinics in affected neighborhoods as well as encourage and support a wider variety of providers (e.g., primary care and general ob-gyn). In addition, although the clinics within this study were able to decrease the stigma associated with visiting an HIV clinic by redefining themselves as community/neighborhood clinics, not all patients will be willing to obtain routine care at an HIV clinic, therefore, access through additional clinic sites remains vital.
There are a number of limitations that should be considered when interpreting the results of this study. Providers with more positive attitudes toward PrEP may have been more inclined to participate in our study. This may have led to selection bias and a reduced likelihood that adverse experiences were captured, but these positive experiences are more likely to reveal more successful tactics. Recruitment was limited to HIV providers within the MSHS that has clinics in New York City that served more racially and ethnically diverse communities. Although these demographics are not universally applicable, these results may be relevant for other diverse urban centers with a high burden of HIV incidence, such as Atlanta or Miami. 24
Disseminating PrEP as a major method of HIV prevention remains limited in the United States, but recent calls by the federal government and physicians for the end of HIV have renewed focus on PrEP, including plans to expand access within primary care and community clinics. 25,26 Although primary care clinics may appear to be the most logical locations for dissemination, HIV clinics provide insight into methods of incorporating PrEP successfully into a multidisciplinary clinic model using a targeted approach that addresses common barriers with clear protocols. The HIV clinic model also demonstrates that funding that supports multidisciplinary teams and addresses gaps in financial support, beyond cost of medication, will help expand PrEP access and combat systemic, provider, and patient-related barriers to PrEP uptake. HIV clinics may also be able to assist other providers, particularly PCPs, by acting as resources and potentially providing training, which would encourage increased provision of PrEP in the primary care setting. Although it may be counterintuitive to the belief that PrEP provision should be spearheaded by PCPs who serve an HIV-negative population, it is clear that HIV and ID clinics can serve as role models in effective PrEP provision and should play a significant role in promoting use of PrEP.
Footnotes
Acknowledgments
The authors thank Dr. Judith Aberg, Christopher Ferraris, LMSW, and the Institute for Advanced Medicine, Mount Sinai Health System, for their assistance in development of the study as well as the study participants for their time and insight.
Disclaimer
The contents do not represent the views of the US Department of Veterans Affairs or the United States Government.
Author Disclosure Statement
No competing financial interests exist.
Funding Information
T.C.K. is supported by the VA Office of Academic Affiliations through the National Clinician Scholars Program.
