Pre-Exposure Prophylaxis (PrEP) Uptake among Black Men Who Have Sex with Men (BMSM) in the Southern U.S.

Black men who have sex with men (BMSM) living in the United States (U.S.) South are disproportionately affected by HIV and experience significant disparities in HIV incidence, access to HIV care, and prevention across ages and socio-economic statuses. The aim of this commentary is to critically review current literature on the state of PrEP use among BMSM in the U.S. South, including identifying barriers and facilitators to PrEP use in order to inform intervention development. Extant literature shows that despite the documented benefits of PrEP as an effective HIV-prevention method, its uptake among BMSM is limited across the U.S. South. Common barriers to PrEP uptake included stigma, homophobia, mistrust of healthcare systems, negative attitudes from healthcare providers, access and transportation issues, poverty, and misinformation about PrEP. These barriers are likely to have been further exacerbated by the COVID-19 pandemic. Limited access to PrEP and other HIV-prevention programs, such as HIV testing, post-exposure prophylaxis (PEP), and condoms for BMSM are likely increase HIV incidence in this community. Moreover, the rapid expansion of telehealth services during the COVID-19 period may offer increased opportunity to scale-up PrEP through telehealth interventions, especially if in-person services remain limited due to pandemic precautions. Given the intersectional barriers that limit the access and uptake of PrEP among BMSM, we suggest that tailored programs or interventions that seek to address PrEP disparities among Southern BMSM should adopt intersectional and interdisciplinary approaches to better understand the complex challenges of scaling up PrEP. More studies are needed to investigate the impact of COVID-19 on HIV-prevention services among BMSM and to understand how to co-develop—with the BMSM community and healthcare providers—culturally acceptable interventions to reduce the identified challenges using intersectional and interdisciplinary approaches.


Introduction
The United States (U.S.) federal government launched the "Ending the HIV Epidemic: A Plan for America" (EHE) initiative in 2019 with the goal of ending the HIV epidemic by 2030 [1]. Six of the seven states identified as key statewide targets in the EHE initiative due to a disproportionate occurrence of HIV in rural areas are in the South [2,3]. The South is home to 38% of the U.S. population but accounted for more than half of all new HIV diagnoses in 2018 [4]. Additionally, the rate of AIDS diagnosis (10.3 per 100,000) was higher in the "Deep South" than in the U.S. general population (6.7 per 100,000) [3]. The EHE initiative prioritizes wider pre-exposure prophylaxis (PrEP) coverage, especially among populations at higher risk of HIV, including Black men who have sex with men

BMSM PrEP Uptake in the South
Prior studies in the U.S. have investigated trends in PrEP use across different regions [3,7,[17][18][19]. A recent analysis of 3108 counties across the U.S. showed that PrEP use was slightly higher in 2018 when compared to 2012 [7]. However, lowest prevalence of PrEP uptake was observed primarily in states in the South: Georgia, Kentucky, North Carolina, South Carolina, Virginia, and West Virginia [7]. Noticeable gaps exist between the willingness to use PrEP and its uptake across the U.S. [3,5,7,8]. Between 2014 and 2015, 68.8% of 333 BMSM surveyed in the American Men's Internet Survey were willing to use PrEP, but only 7.5% used PrEP in the previous year [20]. Similarly in 2017, a national behavioral survey conducted in 23 U.S. cities revealed that 78.3% of BMSM were aware of PrEP, but only 18.8% had used it [21]. A recent national survey conducted with young BMSM (n = 147) revealed that 52% of participants reported that they were likely to be infected with HIV, 39% had heard about PrEP, and 62% disclosed their sexual orientation to healthcare providers and were willing to take PrEP; however, only 8% reported having taken PrEP [22]. In a study conducted with 778 HIV-negative MSM in Atlanta, Detroit, and New York City, 31.2% reported currently taking PrEP, 7.6% previously used it, and 61.2% had never used PrEP due to health concerns (safety), cost, availability, and individual needs [23]. To close the gaps between PrEP knowledge, willingness, and actual usage among BMSM, efforts must be directed towards identifying specific barriers to PrEP uptake and address these barriers through tailored interventions and PrEP campaigns for BMSM given that only a few of the extant strategies to improve PrEP awareness and uptake focus on BMSM [5][6][7].
Surveillance data from 2015 showed that an estimated 1,144,550 million adults had indications for PrEP use [8]. The majority of these "eligible candidates" for PrEP use were MSM (71.1%) when considering likely sources of HIV risk, with Black individuals (43.7%) having the highest indications for PrEP use across races [8].The indication (i.e., PrEP eligibility) for adult MSM was based on individual's negative HIV serostatus diagnosis, being sexually active with multiple male partners, and having exposure to risks (e.g., unprotected anal sex) that could increase their chances of acquiring HIV. For the current review, we extracted the Southern states' data (see Tables 1 and 2) from nationally representative CDC data to show the number of eligible adults and BMSM who had indications for PrEP in 2015. Table 1 shows the total number of all adults in the general population and the estimated number of HIV-negative MSM with PrEP indications (by transmission risk group) across the 16 Southern states and the District of Columbia. Table 2 indicates the total number of Black/African American adults as well as total number of BMSM with PrEP indications (by race/ethnicity) in the South. Indications for PrEP use was high among BMSM (60%) compared to all Black/African American adults who were estimated to be good candidates for PrEP in the South. However, the analysis of 2017 nationally representative data showed poor uptake of PrEP in the Southern U.S. [3]. The high number of PrEP indications among Southern adults-particularly BMSM-did not translate to PrEP uptake across the Southern states, as shown in Table 3. For example, of the 9040 adults in South Carolina who had indications for PrEP, only 590 (6.5%) were prescribed PrEP in 2017 [3]. Thus, while the South has the highest proportion of people living with HIV and higher number of PrEP indications, there is low PrEP uptake [7,24]. This shows that many of those who could potentially benefit from PrEP are not in care and suggests that current national goals to end the HIV epidemic will be difficult to achieve without concerted efforts to enhance PrEP use among Southern individuals at risk for HIV.    Barriers to PrEP Uptake among BMSM in the U.S. South Stigma is a major barrier to PrEP initiation among BMSM who may anticipate and/or encounter negative experiences with healthcare providers, such as being labelled as "promiscuous" when attempting to obtain PrEP [6,25,26]. Recent studies reported that BMSM are less likely to access PrEP and less likely to disclose their sexual identity and sexual behaviors to healthcare professionals due to stigma [16,22,27,28]. HIV-related stigma is high in the South, and PrEP could be associated with HIV risk or an HIV-positive status, which furthers create barriers for uptake [8,26,29]. Other barriers to effective uptake of PrEP among BMSM include mistrust in healthcare systems and socio-structural barriers, such as poverty, racism, and homophobia [5,8]. For example, BMSM in the South are disproportionately affected by poverty, and the refusal of many Southern state legislatures to expand Medicaid benefits to low-income residents has exacerbated existing health and healthcare disparities [14,30]. Additionally, one in eight MSM eligible for PrEP in the South lived between 30-60 min' drive from the providers, and access issues due to transportation are common [3]. Furthermore, there are inconsistencies in how providers assess HIV risk factors and PrEP candidacy among BMSM [5,31]. For example, a 2017 study conducted in six Southeast states among healthcare providers (n = 820) revealed that 52.3% had no knowledge of PrEP, and only 18.1% had prescribed PrEP [32]. A recent study from South Carolina revealed similar findings, where healthcare providers missed opportunities to offer PrEP during healthcare visits to populations at risk, including BMSM [33]. Generally, socio-structural barriers (e.g., stigma, racism, homophobia, poverty) are major impediments to PrEP use among BMSM, thereby exacerbating HIV-related disparities in the South. These challenges therefore call for multilevel interventions to control the HIV epidemic and promote HIV prevention among BMSM in the South.

Impact of COVID-19 on Uptake and PrEP-related Research among BMSM
Although the EHE initiative was welcomed by scientists, funders, politicians, and other key stakeholders, the emergence of the coronavirus (COVID-19) pandemic created unforeseen challenges to meeting EHE goals. Given the nature of the virus, governments across the globe enacted mitigation measures, such as physical distancing and lockdowns, to curb the spread of the virus. Recent studies showed that COVID-19 negatively impacted HIV care and prevention services [2,[34][35][36]. A national survey of MSM was conducted in April 2020; of 204 MSM who reported PrEP use, more than half (68.6%) reported not having any challenges getting a PrEP prescription, 8.8% had problems getting PrEP prescriptions, and 22.5% did not try to access PrEP at all [34]. Importantly, most participants in the survey were non-Hispanic White and had private health insurance, which may have facilitated their access to PrEP during the COVID-19 shutdown [34]. Similarly, Santos and colleagues reported that COVID-19 interrupted most MSM's access to PrEP across the countries sampled (including U.S.) [35]. These findings showed the impact of COVID-19 on MSM access to PrEP and this may potentially increase health inequities among Black individuals in the South.
Furthermore, COVID-19 pandemic restrictions have also affected PrEP-related research in the Southern U.S. We conducted a rapid review of scientific literature (using PubMed and Google Scholar) of empirical studies on PrEP use among BMSM in the U.S. South published between January 2019 and May 2021 to specifically identify any studies published since the EHE initiative was announced as well as during COVID-19 pandemic. Of over 250 articles sampled, only 51 articles reported data partially or wholly collected in the South among BMSM. Although the articles were published between 2019 and 2021, most of the data reported were collected between 2012 and 2017, with only a few studies reporting data from 2018 and 2019 and no studies reporting data collected in 2020 or 2021. Although there is often a lag between data collection and dissemination, this shows the need for more recent data to adequately inform PrEP efforts among BMSM in the South. Since the declaration of EHE initiative in 2019 to eradicate the HIV epidemic within 10 years, few HIV studies have been conducted that focus specifically on BMSM [37]. While COVID-19 disruptions exacerbate the existing health disparities and barriers that inhibit access to PrEP, there is generally a dearth of data on PrEP uptake, retention, and adherence among BMSM in the U.S. [34,35,37,38].
In addition, some scholars have noted that the production of knowledge in the field of public health has mostly been rooted in biomedical research and theories, and it is yet to adopt intersectional and interdisciplinary approaches especially for HIV-related research among BMSM to address health disparities in U.S. [2,37,[39][40][41]. The advancement of studies and interventions that adopt intersectional and interdisciplinary approaches to investigate health disparities, PrEP use, and adherence among BMSM is critical to ending the HIV epidemic in U.S. [34,38,42,43]. For example, HPTN 073 adopted intersectional approaches (e.g., addressing contextual and structural factors that impede on PrEP initiation and adherence among BMSM) to reach BMSM and showed high PrEP initiation among this group at risk of acquiring HIV [38,42]. It is therefore imperative for future studies to adapt intersectional approaches to have a better understanding of barriers and facilitators of PrEP use among BMSM in the South.

Conclusions and Key Recommendations
Historically, BMSM are disadvantaged within the health systems and underrepresented in HIV-related research. Intersectional stigma, racism, homophobia, and poverty must be addressed to improve uptake of PrEP among BMSM in the South. Additionally, there is an urgent need for PrEP promotion to reduce stigma surrounding this prevention strategy and address the myths and misinformation about PrEP, especially in BMSM community. Healthcare systems' strengthening, such as healthcare providers' training, awareness of systemic racism, and sensitization about sexual identity, must be prioritized. In agreement with some scholars [37,38], we recommend that any tailored programs or interventions that seek to address health disparities and contextual and structural factors inhibiting BMSM uptake of PrEP should adopt intersectional and interdisciplinary approaches for better understanding of the problems in order to develop culturally acceptable multilevel interventions. To achieve optimal improved health outcomes among BMSM, the community must be well represented in scientific research or programs on the issues that affect them. Furthermore, the rapid expansion of telehealth services during the COVID-19 period may offer increased opportunity to scale-up PrEP through telehealth interventions/services (e.g., Nurx©, Plushcare©), especially if in-person services remain limited due to pandemic precautions. Accelerating the expansion of PrEP for BMSM in the South (especially those living in rural areas) is critical to achieving the strategic goals of the EHE initiative. Additional studies are also needed to investigate the impact of COVID-19 on HIV-prevention services among BMSM to understand how this community has been affected by the current pandemic as well as to co-develop culturally acceptable multilevel interventions to reduce the identified challenges using intersectional and interdisciplinary approaches.