A survey of South Carolina pharmacists' readiness to prescribe human immunodeficiency virus pre-exposure prophylaxis

Introduction: Human immunodeficiency virus (HIV) pre-exposure prophylaxis (PrEP) is largely underutilized in the Southern United States. Given their community pres-ence, pharmacists are well positioned to provide PrEP within rural, Southern regions. However, pharmacists' readiness to prescribe PrEP in these communities remains unknown. Objective: To

The Southern US has been the region of lowest PrEP use nationally 4 and six of seven key states targeted by the EHE initiative are from this region. 5 South Carolina (SC) is recognized as a state for the EHE initiative due to the disproportionate occurrence of HIV in rural areas. 5 With an estimated 10 249 persons aged ≥16 who were eligible for PrEP, yet only 11.7% of them receiving the medication in 2018, 6 SC is in critical need of creative ways to facilitate PrEP dissemination throughout the state.
While there are many potential barriers to PrEP use, a key factor is patients' access to providers able to prescribe the medication. PrEP is typically offered at academic healthcare centers and clinics offering sexual health services. 7 However, many eligible patients reside in regions with limited access to these specialized locations. A potential solution is the initiation of PrEP through local pharmacies. Pharmacies are a prime location for implementing PrEP services as they are community-facing with wide geographic dispersal. The CDC describes pharmacies as a more accessible and less stigmatizing location for HIV testing and estimates that 70% of rural residents live within 15 miles of a pharmacy and 90% of urban residents live within 2 miles of a pharmacy. 8 In addition, pharmacists have reported that they are well positioned to play a key role in preventing HIV making them a suitable target for PrEP implementation. 9 In December 2021, the Biden Harris National HIV/AIDS strategy outlined these very structural barriers, including state or local laws, and suggests expanding prescribing authority and reimbursement of services for PrEP and post exposure prophylaxis (PEP) to pharmacists. 10 In 2019, California became the first state to pass legislation to allow pharmacists to prescribe PrEP, and Colorado, Nevada, Oregon, Washington, Maine, Virginia, and New Mexico followed shortly thereafter. 11 Despite the need for novel access points for PrEP and the promising aspect of expanding pharmacists' scope of practice, few studies have investigated the feasibility of providing PrEP in a pharmacy setting. A recent systematic review found no published articles comparing the effectiveness of PrEP initiation or continuation through pharmacies. 12 However, there is an increasing number of noncomparative studies showing the feasibility and/or describing a pilot implementation in which PrEP is offered through pharmacies in various geographic regions of the United States including the South. [13][14][15][16][17] Similarly, a recent scoping review supported the feasibility of pharmacy-based interventions to increase PrEP use and its acceptability among potential PrEP users. 18

| METHODS
We distributed a 43-question online descriptive questionnaire to pharmacists licensed to practice in SC using Qualtrics survey software could only select one response. All demographic questions were selfreported. The survey was designed to take less than 15 min to complete. All responses were confidential. During the development, we cognitively field-tested the survey to evaluate flow, comprehension, and duration of the survey. Field-testing participants were practicing pharmacists who were not members of the study team and were ultimately not eligible to participate in the final survey. We also specifically examined responses from rural-based pharmacists as supported by the EHE initiative.
We distributed the email survey invitation hyperlink through the University of South Carolina Kennedy Pharmacy Innovation Center's listserv of licensed pharmacists in SC. The initial invitation was delivered on September 22, 2020, with a reminder email sent on October 9, 2020, with data collection ending on October 17, 2020. The data were collected using Qualtrics survey software which has features to identify duplicate responses. We did not aim to recruit a sample representative of all pharmacists in SC but rather to offer the survey to pharmacists across the state. To encourage participation, all pharmacists were eligible to enter a drawing for one of three $50 gift cards.
At the beginning of the survey, participants were informed of the study procedures to keep their responses confidential and that their participation in the survey was voluntary. Winners were selected using a random number generator and notified via email. Pharmacists

| Participants
Of the initial 2680 unique email addresses to which we distributed the survey, 200 were returned as undeliverable. A total of 150 pharmacists participated in the survey, with 129 completing the full survey and 21 partially completing the survey. No duplicate responses were identified. The majority of pharmacists were female (62%, n = 93), White (73%, n = 110), and non-Hispanic (83%, n = 125) ( Table 1).
3.4 | Feasibility and acceptability of providing PrEP services  Overall, 72% of pharmacists (n = 97/134) thought that a pharmacy was an appropriate location to provide PrEP services. Rural pharmacists felt similarly on the appropriateness of pharmacies for PrEP. In the free response sections of the survey asking why pharmacies are an appropriate place to prescribe PrEP, pharmacists stated: "Pharmacies are accessible to anyone off the street. There are many barriers, some perceived, to getting a patient seen by a physician" and "Patients are more likely to come to the pharmacy before seeking care from a physician" and "Prescribing PrEP at a pharmacy will allow more patients to have access to care and pharmacists/pharmacy interns are able to provide proper counseling and follow-up".

| Readiness to provide PrEP care
A large proportion of pharmacists (60%, n = 79/130) reported being at least somewhat ready to provide PrEP services including 65% of rural pharmacists. Barriers to providing PrEP care from most to least reported included costs, lack of staff knowledge with PrEP, insurance status of patient, lack of time, lack of comfort prescribing PrEP, and concerns regarding the side effects of PrEP ( Figure 4A). Pharmacists also indicated in free-response answers that patient follow-up visits, staffing limitations, liability, and communication with providers were potential barriers. One pharmacist noted, "We are a small pharmacy with only one pharmacist on duty at a time. We also have limited space for counselling. This type of program would need more staff and more space than we have available". To overcome these obstacles, pharmacists requested additional trainings, guidelines, medical provider assistance, and experience with the medication ( Figure 4B).
The vast majority of pharmacists (86%, n = 111/129), including 94% of rural pharmacists, stated they would be willing to prescribe PrEP. interpretation, and how PrEP can be used for HIV prevention. 8,24 In addition, the CDC provides guidelines to help prescribers determine who is eligible to be started on the medication. 25 Regional AIDS Education and

| DISCUSSION
Training Centers can play a key role in expanding awareness and building capacity for PrEP implementation. There are also resources specifically for pharmacists implementing PrEP into their practice. 26 Educational efforts such as these have been effective in increasing PrEP prescriptions among Southern primary care providers. 27 Pharmacists are already providing preventative services such as providing unused syringes and naloxone to persons who inject drugs, prescribing and administering injectable and self-administered hormonal contraceptives, HIV and hepatitis C testing, blood glucose monitoring for diabetes, and cholesterol and blood pressure checks for cardiovascular disease. [28][29][30] More recently, pharmacists have been allowed to prescribe nirmatrelvir/ritonavir with the Emergency Use Authorization during the COVID pandemic. 31 As pharmacists' scope of practice expands with prescriptive authority, 32,33 pharmacists may prescribe PrEP and HIV PEP in certain states. 34,35 Unfortunately, SC law does not currently allow pharmacists the ability to provide PrEP, limiting their ability to provide this vital preventative service. Collaboration with policy makers is needed to expand the scope of practice of SC pharmacists to include PrEP prescribing and allowing local pharmacies to serve as access points for HIV preventative services.
Affordability of the medication is also a common concern when managing PrEP. Patient assistance programs exist such as the federal Ready, Set, PrEP program that work with pharmacies to provide PrEP at no cost to patients. 36 Pharmacists play a key role in managing health care costs for their health systems and patients. 37 They often have experience managing prior authorizations, insurance claims, out-of-pocket costs, and completing patient assistance applications for the patients they serve.
Pharmacist-driven medication therapy management, including for HIV care, has resulted in improved patient outcomes and costs. 38 Another barrier to PrEP implementation at pharmacies is the time commitment needed to counsel, test, and start a patient on PrEP. Pharmacists are frequently overburdened which can limit the amount of time they have to spend with a patient and lead to potential adverse events. 39 In addition, their pharmacy may not have confidential areas to privately discuss PrEP in a pharmacy setting. 40 These concerns may be partially mitigated by the route that the patient prefers to access the pharmacy. A prior study demonstrated that patients tend to obtain confidential prescriptions through drive-through pharmacies, but are more open to counseling when entering the pharmacy in-person. 41 Still, pharmacies that plan to begin providing PrEP services will need to allow for adequate time and a confidential location for pharmacists and patients to discuss PrEP based on their own unique practice structure and layout.
Pharmacists also had concerns about PrEP leading to increased high-risk sexual encounters which in turn may lead to increased STI transmission rates in their patients. This a valid concern as PrEP has been associated with increased STI rates. 42 This is especially important in SC which was ranked as the fourth-highest state for reported rates of chlamydia and third-highest state for reported cases of gonorrhea in 2020. 43 Fortunately, pharmacists are uniquely situated to help reduce the surge of infections. Prior studies have shown that pharmacists can reduce time to therapy and ensure optimum therapy for patients with STIs. 35 In addition, patients have found pharmacistled testing for and managing of STIs to be acceptable. 44 Limitations to our study include a low response rate. Our aim was to collect descriptive data from a sample of pharmacists from a variety of practice locations and pharmacy types across SC on their readiness to provide PrEP. However, the response rate achieved is typical for surveys administered in the manner we used including those for medical providers and pharmacists. 45,46 Yet, surveys with low response rates can still provide quality and useful data, especially when the aim of a study is to gather information to help inform subsequent interventions, such as ours. 47  only able to select one practice location and type in our survey, while it is very possible that pharmacists were working in multiple settings or having overlap between pharmacy sites. In addition, we did not define the different pharmacy practice settings offered in our survey. By allowing pharmacists to choose which option best described their pharmacy practice, there may be discrepancies in how different pharmacists interpret their workplace. Our survey was also administered prior to the 2021 update to the CDC PrEP guidelines which updated eligibility criteria for PrEP and ways to provide PrEP counseling. 25 Ultimately, our formative results can help provide a framework toward a pharmacist-driven PrEP model which can then be disseminated and used to create a PrEP program among pharmacists in SC. However, the generalizability of this model and pharmacist prescribing practice to other states is ultimately dependent upon individual state laws.

| CONCLUSION
To our knowledge, this was the first survey of SC pharmacists on their viewpoints surrounding providing PrEP services. In our sample, pharmacists believed that PrEP was beneficial, and that the pharmacy was a feasible and acceptable location for providing PrEP services.
The majority of surveyed pharmacists were willing to prescribe PrEP if allowed. However, further educational programs may be needed to prepare and support pharmacists in providing PrEP services. We will use these data, coupled with data from a subsequent qualitative descriptive study we conducted with selected survey participants, to begin the development of a framework for pharmacists to deliver PrEP in the South. Ultimately, the decision to allow SC pharmacists to prescribe PrEP will be made by the SC legislature. However, it is our hope that real-world data from our survey, combined with the new National HIV/AIDS Strategy, will help the needle move in the right direction. We are hopeful that increasing PrEP access through pharmacies will provide this highly effective HIV prevention medication to persons at risk for HIV and who may not have had access previously.