- Email: [email protected]
Engaging United States Black Communities in HIV Pre-exposure Prophylaxis: Analysis of a PrEP Engagement Cascade
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Engaging United States Black Communities in HIV Pre-exposure Prophylaxis: Analysis of a PrEP Engagement Cascade Helena Akua Kwakwa, M.D., M.P.H., Sophia Bessias, M.P.H., Donielle Sturgis, M.P.H., Gina Walton, B.A., Rahab Wahome, M.P.H., Oumar Gaye, M.D., M.P.H., Mayla Jackson, M.P.H.
INTRODUCTION Conflicts of interest: We report no funding source for this study. Acknowledgements: This research was supported by a grant from the Centers for Disease Control and Prevention Foundation. Abstract: Background/Purpose: National PrEP utilization analyses show US nonHispanic Blacks accessing PrEP at disproportionately low rates given the higher HIV prevalence among Blacks, and in comparison to utilization by non-Hispanic Whites. Women also are underrepresented among PrEP utilizers, especially Black women. We examine the process of accessing PrEP for a majority Black population in an urban community health center setting. Methods: In the Philadelphia city health centers, patients referred for PrEP were followed through six steps of accessing PrEP: referral, patient contact by a PrEP team, maintained interest by patients, scheduling of screening appointments, attending screening appointments, and initiating PrEP. Chi-squared tests were performed at each stage to identify gender differences in drop-off at each step. Results: Between August 2014 and December 2015, 14% of 785 patients referred for PrEP initiated. Women constituted 37.8% of referrals. A smaller majority of Blacks initiated (84.6% of females, 69.5% of males) than were referred (94.5% of females, 88.1% of males). Prior knowledge of PrEP was associated with screening (68% of those with prior knowledge screened, compared with 29.6% of those without prior knowledge,Χ2 p<0.0001). Higher initiation:referral ratios were noted for self-referrals, and for those referred by clinicians, peers and partners. Conclusions: In a diverse cohort in a community health center setting, myriad barriers resulted in a 14% initiation rate for persons at elevated risk for HIV who were referred for PrEP. These barriers led to disproportionately fewer nonHispanic Blacks and women initiating PrEP. Efforts to better engage Blacks and women in PrEP care are urgently needed, and may include better dissemination of PrEP-related information in Black communities and to women, and training of clinicians serving Black and female populations to improve competency in provision of PrEP care. Keywords: HIV-PrEP-Engagement-Cascade-Black
Author affiliations: Helena Akua Kwakwa, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Sophia Bessias, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Donielle Sturgis, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Gina Walton, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Rahab Wahome, AIDS Care Group, 907 Chester Pike, Sharon Hill, PA 19079, USA; Oumar Gaye, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Mayla Jackson, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA Correspondence: Helena Akua Kwakwa, M.D., M.P.H. Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 S. Broad St., Philadelphia, PA 19146, USA., email: [email protected] Published by Elsevier Inc. on behalf of the National Medical Association.
https://doi.org/10.1016/j.jnma.2017.12.006
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DF/FTC for HIV pre-exposure prophylaxis (PrEP) is a safe and highly effective method of HIV prevention.1e5 As such, it has the potential, used with other prevention methods, to control the HIVepidemic in the most impacted US communities in ways that decades of barrier protection, behavior change, routine testing and treatment have not. Yet five years following the approval of TDF/FTC for PrEP,6 uptake among racial and ethnic minority populations remains low relative to the rate of new infections in these highly impacted groups. Uptake in minority communities also remains low relative to nonminority populations who have seen substantial increases in uptake in recent years.7e15 In 2015 Blacks constituted 45% of estimated new HIV infections in the US,16 yet between 2012 and 2015 only 10% of PrEP users were Black.17 It is estimated that should our current epidemic trajectory continue, one in nineteen Black men, including one in two Black men who have sex with men (MSM) will be diagnosed with HIV in their lifetime.18 Although Hispanics accounted for 24% of new US infections in 2015,16 a disproportionately low 12% of PrEP users were Hispanic.17 Among Hispanic men, one in forty-eight, including one in four MSM will be diagnosed with HIV in their lifetime should our current course continue unchanged.18 On the other hand, White Americans, 27% of estimated new US infections in 2014,16 represented 74% of PrEP utilizers through September 2015.17 Among White men one in 127, including one in eleven MSM will be diagnosed with HIV in their lifetime.18 PrEP utilization by US women has also been low. The number of female PrEP users has remained low and relatively stable between 2012 and 2015, as utilization by men has grown at an increasing pace. Hence the percentage of PrEP utilizers who are female has declined from 48.5% in 2012 to 11.4% in the third quarter of 2015.17 Approximately
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one in five new HIV infections in 2015 occurred in women.16 Furthermore, compared with White women, Black women are 20 times more likely to have HIV infection,16 but between 2012 and 2015 Black women were over four times less likely to have initiated PrEP compared to White women.17 According to published estimates by Smith et al, 624,000 heterosexually active adults in the US meet risk criteria for PrEP, 468,000 of whom are women.19 This estimate rivals the estimated 492,000 MSM meeting criteria for PrEP in the same analysis. It would appear that some communities most in need of effective HIV prevention are not accessing one of the most effective prevention methods available. Strategies to engage communities of color, including women of color, in PrEP utilization are urgently needed. As an important step to this end we examine the process of PrEP engagement for a clinic population consisting primarily of racial/ethnic minorities in urban US, examining barriers and facilitators at each step of the engagement process in an effort to determine successful strategies to engage communities of color in PrEP.
METHODS In August of 2014 the Philadelphia city health centers implemented a structured clinical PrEP program for existing and referred patients at high risk for HIV. The city health centers are Federally Qualified Health Center (FQHC) look-alike facilities in Philadelphia. Each center offers comprehensive primary care services as well as HIV specialty services. Residents of Philadelphia are eligible to receive these services regardless of insurance status or ability to pay, but insured patients requiring capitation must select a health center as a primary care provider (PCP) in order to receive services. In Fiscal Year 2016, 46.2% of patients receiving services at the health centers were uninsured (Data on file). As a part of the PrEP program, referrals were solicited from health center staff as well as from community providers of HIV testing services. A PrEP team was notified about all referrals, and attempted to reach referred patients within 24 hours. Patients expressing maintained interest in PrEP were scheduled appointments, and attended these appointments for screening. They were then started on PrEP if they were medically eligible. The median time between referral and initiation of PrEP was 5 days. The following six steps were delineated for PrEP engagement: 1. Referral for PrEP services; 2. Contact with referred patient by PrEP team; 3. Maintained interest in PrEP expressed by contacted patient; 4. Appointment scheduled for PrEP screening;
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Figure 1. PrEP Referral Outcomes by gender, Philadelphia City Health Centers, August 2014eDecember 2015. 600 500 400 300 200 100 0 Referred
Contacted
Interested Women
Scheduled
Screened
Iniated
Men
5. Screening appointment completed; 6. PrEP initiated. Chi-squared tests were performed at each stage to identify gender differences in progressing through each step of accessing PrEP. Patient referral outcomes by referral source were evaluated, with the percentage of PrEP initiators determined and reported by referral source. Referral outcomes were also evaluated by prior knowledge of PrEP. Data for this study were analyzed in R version 3.2.4.20 This study was approved by the City of Philadelphia Institutional Review Board.
RESULTS AND DISCUSSION Results Between August 2014 and December 2015, 785 patients were referred for PrEP, 297 of whom were female (37.8%), and 485 male (61.9%). The median age was 27 years for women and 26 years for men. Of 664 referred patients with known insurance status (84.6% reporting), half (50.0%) were uninsured, with women more likely to be insured than men (57.3% vs. 38.7%, p < 0.0001). The vast majority of patients first learned about PrEP during the referral process. Of 408 patients responding to the question, 85 (20.8%) had heard of PrEP prior to the encounter resulting in a referral. Of the 785 referred patients, 110 initiated PrEP. Almost a quarter (23.6%, n ¼ 26) of initiators were female, and three quarters (74.5%) were male. Figure 1 shows the number of individuals, by gender, engaging in each step of the process of accessing PrEP. It shows substantial drop-off from referral to initiation regardless of gender. Between referral and patient contact we found a greater than 30% drop-off (485 referred and 312 reached (64.3%) for men, and 297 referred and 189 reached (63.6%) for women). Although the drop-off was not as substantial, there was a statistically significant gender difference in maintained interest at the time of
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Table 1. Rates of screening for PrEP by prior knowledge of PrEP and by gender, Philadelphia City Health Centers, August 2014eDecember 2015.
Did not proceed with screening, n (%)
Screened, n (%)
No prior knowledge of PrEP
131 (70.4%)
55 (29.6%)
Prior knowledge of PrEP
24 (32.0%)
51 (68%)
Prior knowledge of PrEP, and gender All*
Women** No prior knowledge of PrEP
44 (65.7%)
23 (34.3%)
Prior knowledge of PrEP
3 (25%)
9 (75.0%)
Men* No prior knowledge of PrEP
87 (73.7%)
31 (26.3%)
Prior knowledge of PrEP
21 (33.3%)
42 (66.7%)
*c2 p < 0.0001. **Fisher p ¼ 0.01.
reaching the patient (90.7% of men and 79.9% of women maintained interest, p < 0.01). Women were also less likely than men to schedule appointments (p ¼ 0.02), but of those scheduling appointments there was no gender difference in attendance at appointments and completion of screening (265 scheduled and 112 completed (42.3%) for men, and 136 scheduled and 58 completed (42.6%) for women). However for women there was another substantial drop-off between completion of screening and initiating PrEP (58 screened and 26 (44.8%) initiated), while for men this drop-off was less (112 screened and 82 (73.2%) initiated). Race and ethnicity were reported for 551 referrals (70.2% reporting) and for all initiators. Among referred women 94.5% (n ¼ 224) were Black non-Hispanic, and a minority were White non-Hispanic and Hispanic (2.6%, n ¼ 6, and 2.9%, n ¼ 7 respectively). Of 26 female PrEP initiators, a smaller majority (84.6%, n ¼ 22) were Black non-Hispanic, and a minority were White non-Hispanic, and Hispanic (7.7%, n ¼ 2 for both). For referred men, 88.1% (n ¼ 275) were Black non-Hispanic, 7.7% (n ¼ 24) were White non-Hispanic, and 4.2% (n ¼ 13) were Hispanic. Comparing 78 male initiators to referred men, a smaller majority (69.5%, n ¼ 57) were Black non-
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Table 2. Percentage initiating PrEP by referral source, Philadelphia City Health Centers, August 2014eDecember 2015.
Referral Source
Number Referred
Number and Percentage of Referred Initiating PrEP
HIV Rapid Tester
617
44 (7.1%)
Self, peer or partner
23
14 (60.9%)
Clinician
61
30 (49.2%)
Community Organization
23
5 (21.7%)
Navigator
35
11 (31.4%)
Total
759
104 (13.7%)
Hispanic, while a larger minority were White nonHispanic (19.5%, n ¼ 16) and Hispanic (6.1% n ¼ 5). Table 1 shows referral outcomes for those referred by gender and by prior knowledge of PrEP. Overall those with prior knowledge of PrEP were significantly more likely to complete the process of screening for PrEP. While fewer than a third (29.6%) of those with no prior knowledge of PrEP were screened, more than two thirds (70.4%) of those with prior knowledge went on to screen for PrEP (X2 p < 0.0001). This pattern held true for women (75.0% with prior knowledge, 34.3% without, Fisher p ¼ 0.01) and men (66.7% with prior knowledge, 26.3% without, X2 p < 0.0001). Among men 34.8% had heard of PrEP while for women only 15.2% had heard of PrEP prior to their referral (X2 p-value<0.001). The referral source was known for 759 referrals (96.8% reporting). As shown in Table 2, the primary referral source was the health center HIV Rapid Testers. More than three quarters (81.3%) of all referrals were from the Rapid Testers. While only 7.1% of Rapid Tester referrals proceeded to initiate PrEP, these collectively constituted a substantial portion (40.0%) of PrEP initiators. The percentage of Rapid Tester referrals initiating PrEP increased at month 9 of the study when a PrEP team member was located at the busiest testing site one day a week. This increase brought the Rapid Testing referrals who went on to initiate PrEP from 5.6% at 8 months, to 7.1% in this analysis (17 months). The greatest ratios of initiation: referral were observed for clinician and self/peer/partner referrals. Of the 61 persons referred by clinicians, 30 (49.2%) went on to initiate PrEP, and of the 23 self, peer and partner referrals, more than half (60.9%, n ¼ 14) initiated PrEP. Overall, 14.0% of individuals (8.8% of women and 17.3% of men, p < 0.05) referred for PrEP completed the engagement process and initiated PrEP.
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Discussion The United States FDA was the first national regulatory body to approve TDF/FTC for PrEP,6 placing the US in the position of world leader in real world PrEP implementation. National uptake to date suggests that current strategies for implementation have had differential success across racial, ethnic and gender lines, with some communities at highest risk accessing PrEP the least. In a largely Black clinic population in Philadelphia, 61.4% of men and 54.8% of women expressed an interest in PrEP.21 Yet this high level of interest may not necessarily translate into utilization, as suggested by Rolle et al in an observational prospective study of young Black MSM in Atlanta.22 In this latter study only 35% from this high-risk cohort initiated PrEP despite high levels of interest.22 Although a large internet study of MSM noted no difference in reported PrEP utilization by race, authors cautioned that the small number of Black MSM in the study may limit the power to detect differences by race.23 In the Deep South, where Black communities may be the most impacted by HIV, limited PrEP uptake among Black men and women, including Black MSM, is reported.24 This current study provides some data on factors impeding and those facilitating engagement in PrEP for a majority Black cohort in urban US. It is important to note that among presented models of PrEP engagement is sameday PrEP initiation,25 which would theoretically eliminate the drop-off across the engagement cascade. For many settings this same-day start approach may not be feasible, hence these data are of relevance to the discourse on PrEP engagement, and to the discussion of strategies for engagement of racial minorities as well as for women. Gender. In this study initiation rates were higher for men than for women. The higher rates in men were driven in part by greater levels of prior knowledge of PrEP, a factor we found to be highly associated with PrEP initiation. Low levels of PrEP awareness among women have been previously documented. In a group of 39 women participating in focus groups in Washington DC, only 5 had heard of PrEP.26 Media campaigns and other strategies to improve awareness of PrEP especially and specifically in Black communities is a necessary part of increasing access to PrEP. Variations in prior knowledge of PrEP may not fully explain the gender difference in initiation rates. Chisquared tests performed at each stage of the engagement model showed gender differences of statistical significance in scheduling screening appointments. This difference in scheduling screening appointments is explained in part by differences in insurance status. Insured patients reluctant to change their PCP to the health center were not eligible to
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receive PrEP or other services at said health center, paradoxically resulting in a smaller percentage of the insured proceeding to PrEP initiation within our system. Women were statistically more likely to be insured, accounting in part for the gender difference in scheduling appointments. Hence at facilities without the requirement that patients switch their PCP, the gender difference in PrEP initiation rates may be smaller. Indeed, lack of insurance has been reported as a documented barrier to PrEP access in other settings,27 highlighting the nuances of the impact of lack of insurance on access to PrEP by site. For those scheduling appointments, there was no gender difference in screening completion. However, among those completing screening appointments, women were less likely to proceed with PrEP initiation although they were not less likely to be medically eligible. Race and ethnicity. Initiation rates also differed by race and ethnicity. Non-Hispanic Blacks constituted a smaller percentage of initiators than referrals. Conversely, Hispanics and non-Hispanic Whites represented a larger percentage of initiators than referrals. Essentially among a group of high-risk patients referred for PrEP, non-Hispanic Blacks were the least likely to proceed through the engagement process to begin PrEP. This finding has been reported in previous research. Katz et al noted that among MSM in Seattle, levels of engagement were substantially lower for Asian and Black MSM compared to White MSM (21% and 22% respectively compared with 40%).28 The lower rate of completing the process of accessing PrEP for Blacks, a group highly impacted by HIV, in a setting that eliminated lack of health insurance as a barrier, is cause for concern. Research shows that engagement of Black MSM in a client-centered model with care coordination is feasible.29 Further studies such as this are urgently needed to examine successful models, and to evaluate reasons and remedies for differential access by race. Referral source. Table 2 shows the percentage starting PrEP by referral source. The least efficient referral source was the HIV Rapid Testers, 7.1% of their 617 referrals going on to initiate PrEP. Having a member of the PrEP team at the busiest Rapid Testing site one day a week improved the percentage of referred patients from that site who proceeded to screening appointments. HIV testing offers a unique opportunity for the discussion of PrEP, and this discussion may be most impactful at the time of testing. Having trained staff on-site to discuss PrEP as a part of the testing process helps to capitalize on this opportunity. While the percentage of Rapid Tester referrals beginning PrEP was low, they were an essential referral source partly because they reached a population otherwise unengaged in the health care system, partly because the
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sheer volume of referrals was such that even a small percentage constituted a substantial portion of initiators, and also because the nature of their role makes them a natural fit for initiating a discussion about HIV risk and PrEP. Self/peer/partner referrals yielded the highest proportion of initiators, followed by clinician referrals. Patients seeking PrEP as a result of self/peer/partner referrals were a select group highly motivated to seek out PrEP and hence had high rates of completing the access process. Strategies to disseminate information about PrEP directly to communities, and to encourage PrEP referrals within social and sexual networks, will be important in engaging communities at risk in PrEP care. Those referred by a clinician were able to have their clinical questions answered, and begin the process of evaluation for medical eligibility during the same visit, which facilitated their initiation. Clinician recommendations may also have been considered more seriously by patients than recommendations of others, given existing relationships of trust between clinician and patient. Encouraging clinicians to initiate conversations about PrEP with patients is a potentially important component of improving access. PrEP awareness. Participants who were aware of PrEP were substantially more likely to complete the PrEP access process. PrEP awareness campaigns should target all groups at elevated risk for HIV, including communities of color.
IMPLICATIONS In this study, the low percentage of high-risk referred patients who completed the access process and initiated PrEP suggests a need for support and facilitation at each step of the PrEP engagement cascade, particularly for populations with steeper fall-off such as those who have never heard of PrEP, non-Hispanic Blacks, and women. Continuing to monitor the impact of insurance in different settings is important as the insurance landscape undergoes shifts. The domestic HIV epidemic impacts non-Hispanic Blacks to a greater degree than other groups. It is critical that the necessary effort be invested in engaging this community despite a potentially greater degree of difficulty. Should we fail to improve PrEP utilization among racial/ethnic minorities, existing disparities in HIV prevalence stand to grow.
high risk heterosexuals: subgroup analyses from the Partners PrEP Study. AIDS, 27(13), 2155e2160. 3. Grant, R. M., Lama, J. R., Anderson, P. L., et al. (2010). Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med, 363(27), 2587e2599. 4. Choopanya, K., Martin, M., Suntharasamai, P., et al. (2013). Antiretroviral prophylaxis for HIV infection in injecting drug users in Bangkok, Thailand (the Bangkok Tenofovir Study): a randomised, double-blind, placebo-controlled phase 3 trial. Lancet, 381(9883), 2083e2090. 5. Grohskopf, L. A., Chillag, K. L., Gvetadze, R., et al. (2013). Randomized trial of clinical safety of daily oral tenofovir disoproxil fumarate among HIV-uninfected men who have sex with men in the United States. J Acquir Immune Defic Syndr, 64(1), 79e86. 6. United States Food and Drug Administration (FDA). (2012). FDA Approves First Drug for Reducing the Risk of Sexually Acquired HIV Infection. Washington, DC http://www.fda.gov/NewsEvents/ Newsroom/PressAnnouncements/ucm312210.htm.
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Engaging United States Black Communities in HIV Pre-exposure Prophylaxis: Analysis of a PrEP Engagement Cascade Helena Akua Kwakwa, M.D., M.P.H., Sophia Bessias, M.P.H., Donielle Sturgis, M.P.H., Gina Walton, B.A., Rahab Wahome, M.P.H., Oumar Gaye, M.D., M.P.H., Mayla Jackson, M.P.H.
INTRODUCTION Conflicts of interest: We report no funding source for this study. Acknowledgements: This research was supported by a grant from the Centers for Disease Control and Prevention Foundation. Abstract: Background/Purpose: National PrEP utilization analyses show US nonHispanic Blacks accessing PrEP at disproportionately low rates given the higher HIV prevalence among Blacks, and in comparison to utilization by non-Hispanic Whites. Women also are underrepresented among PrEP utilizers, especially Black women. We examine the process of accessing PrEP for a majority Black population in an urban community health center setting. Methods: In the Philadelphia city health centers, patients referred for PrEP were followed through six steps of accessing PrEP: referral, patient contact by a PrEP team, maintained interest by patients, scheduling of screening appointments, attending screening appointments, and initiating PrEP. Chi-squared tests were performed at each stage to identify gender differences in drop-off at each step. Results: Between August 2014 and December 2015, 14% of 785 patients referred for PrEP initiated. Women constituted 37.8% of referrals. A smaller majority of Blacks initiated (84.6% of females, 69.5% of males) than were referred (94.5% of females, 88.1% of males). Prior knowledge of PrEP was associated with screening (68% of those with prior knowledge screened, compared with 29.6% of those without prior knowledge,Χ2 p<0.0001). Higher initiation:referral ratios were noted for self-referrals, and for those referred by clinicians, peers and partners. Conclusions: In a diverse cohort in a community health center setting, myriad barriers resulted in a 14% initiation rate for persons at elevated risk for HIV who were referred for PrEP. These barriers led to disproportionately fewer nonHispanic Blacks and women initiating PrEP. Efforts to better engage Blacks and women in PrEP care are urgently needed, and may include better dissemination of PrEP-related information in Black communities and to women, and training of clinicians serving Black and female populations to improve competency in provision of PrEP care. Keywords: HIV-PrEP-Engagement-Cascade-Black
Author affiliations: Helena Akua Kwakwa, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Sophia Bessias, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Donielle Sturgis, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Gina Walton, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Rahab Wahome, AIDS Care Group, 907 Chester Pike, Sharon Hill, PA 19079, USA; Oumar Gaye, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA; Mayla Jackson, Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 South Broad St., Philadelphia, PA 19146, USA Correspondence: Helena Akua Kwakwa, M.D., M.P.H. Philadelphia Department of Public Health, Division of Ambulatory Health Services, 500 S. Broad St., Philadelphia, PA 19146, USA., email: [email protected] Published by Elsevier Inc. on behalf of the National Medical Association.
https://doi.org/10.1016/j.jnma.2017.12.006
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T
DF/FTC for HIV pre-exposure prophylaxis (PrEP) is a safe and highly effective method of HIV prevention.1e5 As such, it has the potential, used with other prevention methods, to control the HIVepidemic in the most impacted US communities in ways that decades of barrier protection, behavior change, routine testing and treatment have not. Yet five years following the approval of TDF/FTC for PrEP,6 uptake among racial and ethnic minority populations remains low relative to the rate of new infections in these highly impacted groups. Uptake in minority communities also remains low relative to nonminority populations who have seen substantial increases in uptake in recent years.7e15 In 2015 Blacks constituted 45% of estimated new HIV infections in the US,16 yet between 2012 and 2015 only 10% of PrEP users were Black.17 It is estimated that should our current epidemic trajectory continue, one in nineteen Black men, including one in two Black men who have sex with men (MSM) will be diagnosed with HIV in their lifetime.18 Although Hispanics accounted for 24% of new US infections in 2015,16 a disproportionately low 12% of PrEP users were Hispanic.17 Among Hispanic men, one in forty-eight, including one in four MSM will be diagnosed with HIV in their lifetime should our current course continue unchanged.18 On the other hand, White Americans, 27% of estimated new US infections in 2014,16 represented 74% of PrEP utilizers through September 2015.17 Among White men one in 127, including one in eleven MSM will be diagnosed with HIV in their lifetime.18 PrEP utilization by US women has also been low. The number of female PrEP users has remained low and relatively stable between 2012 and 2015, as utilization by men has grown at an increasing pace. Hence the percentage of PrEP utilizers who are female has declined from 48.5% in 2012 to 11.4% in the third quarter of 2015.17 Approximately
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one in five new HIV infections in 2015 occurred in women.16 Furthermore, compared with White women, Black women are 20 times more likely to have HIV infection,16 but between 2012 and 2015 Black women were over four times less likely to have initiated PrEP compared to White women.17 According to published estimates by Smith et al, 624,000 heterosexually active adults in the US meet risk criteria for PrEP, 468,000 of whom are women.19 This estimate rivals the estimated 492,000 MSM meeting criteria for PrEP in the same analysis. It would appear that some communities most in need of effective HIV prevention are not accessing one of the most effective prevention methods available. Strategies to engage communities of color, including women of color, in PrEP utilization are urgently needed. As an important step to this end we examine the process of PrEP engagement for a clinic population consisting primarily of racial/ethnic minorities in urban US, examining barriers and facilitators at each step of the engagement process in an effort to determine successful strategies to engage communities of color in PrEP.
METHODS In August of 2014 the Philadelphia city health centers implemented a structured clinical PrEP program for existing and referred patients at high risk for HIV. The city health centers are Federally Qualified Health Center (FQHC) look-alike facilities in Philadelphia. Each center offers comprehensive primary care services as well as HIV specialty services. Residents of Philadelphia are eligible to receive these services regardless of insurance status or ability to pay, but insured patients requiring capitation must select a health center as a primary care provider (PCP) in order to receive services. In Fiscal Year 2016, 46.2% of patients receiving services at the health centers were uninsured (Data on file). As a part of the PrEP program, referrals were solicited from health center staff as well as from community providers of HIV testing services. A PrEP team was notified about all referrals, and attempted to reach referred patients within 24 hours. Patients expressing maintained interest in PrEP were scheduled appointments, and attended these appointments for screening. They were then started on PrEP if they were medically eligible. The median time between referral and initiation of PrEP was 5 days. The following six steps were delineated for PrEP engagement: 1. Referral for PrEP services; 2. Contact with referred patient by PrEP team; 3. Maintained interest in PrEP expressed by contacted patient; 4. Appointment scheduled for PrEP screening;
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Figure 1. PrEP Referral Outcomes by gender, Philadelphia City Health Centers, August 2014eDecember 2015. 600 500 400 300 200 100 0 Referred
Contacted
Interested Women
Scheduled
Screened
Iniated
Men
5. Screening appointment completed; 6. PrEP initiated. Chi-squared tests were performed at each stage to identify gender differences in progressing through each step of accessing PrEP. Patient referral outcomes by referral source were evaluated, with the percentage of PrEP initiators determined and reported by referral source. Referral outcomes were also evaluated by prior knowledge of PrEP. Data for this study were analyzed in R version 3.2.4.20 This study was approved by the City of Philadelphia Institutional Review Board.
RESULTS AND DISCUSSION Results Between August 2014 and December 2015, 785 patients were referred for PrEP, 297 of whom were female (37.8%), and 485 male (61.9%). The median age was 27 years for women and 26 years for men. Of 664 referred patients with known insurance status (84.6% reporting), half (50.0%) were uninsured, with women more likely to be insured than men (57.3% vs. 38.7%, p < 0.0001). The vast majority of patients first learned about PrEP during the referral process. Of 408 patients responding to the question, 85 (20.8%) had heard of PrEP prior to the encounter resulting in a referral. Of the 785 referred patients, 110 initiated PrEP. Almost a quarter (23.6%, n ¼ 26) of initiators were female, and three quarters (74.5%) were male. Figure 1 shows the number of individuals, by gender, engaging in each step of the process of accessing PrEP. It shows substantial drop-off from referral to initiation regardless of gender. Between referral and patient contact we found a greater than 30% drop-off (485 referred and 312 reached (64.3%) for men, and 297 referred and 189 reached (63.6%) for women). Although the drop-off was not as substantial, there was a statistically significant gender difference in maintained interest at the time of
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Table 1. Rates of screening for PrEP by prior knowledge of PrEP and by gender, Philadelphia City Health Centers, August 2014eDecember 2015.
Did not proceed with screening, n (%)
Screened, n (%)
No prior knowledge of PrEP
131 (70.4%)
55 (29.6%)
Prior knowledge of PrEP
24 (32.0%)
51 (68%)
Prior knowledge of PrEP, and gender All*
Women** No prior knowledge of PrEP
44 (65.7%)
23 (34.3%)
Prior knowledge of PrEP
3 (25%)
9 (75.0%)
Men* No prior knowledge of PrEP
87 (73.7%)
31 (26.3%)
Prior knowledge of PrEP
21 (33.3%)
42 (66.7%)
*c2 p < 0.0001. **Fisher p ¼ 0.01.
reaching the patient (90.7% of men and 79.9% of women maintained interest, p < 0.01). Women were also less likely than men to schedule appointments (p ¼ 0.02), but of those scheduling appointments there was no gender difference in attendance at appointments and completion of screening (265 scheduled and 112 completed (42.3%) for men, and 136 scheduled and 58 completed (42.6%) for women). However for women there was another substantial drop-off between completion of screening and initiating PrEP (58 screened and 26 (44.8%) initiated), while for men this drop-off was less (112 screened and 82 (73.2%) initiated). Race and ethnicity were reported for 551 referrals (70.2% reporting) and for all initiators. Among referred women 94.5% (n ¼ 224) were Black non-Hispanic, and a minority were White non-Hispanic and Hispanic (2.6%, n ¼ 6, and 2.9%, n ¼ 7 respectively). Of 26 female PrEP initiators, a smaller majority (84.6%, n ¼ 22) were Black non-Hispanic, and a minority were White non-Hispanic, and Hispanic (7.7%, n ¼ 2 for both). For referred men, 88.1% (n ¼ 275) were Black non-Hispanic, 7.7% (n ¼ 24) were White non-Hispanic, and 4.2% (n ¼ 13) were Hispanic. Comparing 78 male initiators to referred men, a smaller majority (69.5%, n ¼ 57) were Black non-
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Table 2. Percentage initiating PrEP by referral source, Philadelphia City Health Centers, August 2014eDecember 2015.
Referral Source
Number Referred
Number and Percentage of Referred Initiating PrEP
HIV Rapid Tester
617
44 (7.1%)
Self, peer or partner
23
14 (60.9%)
Clinician
61
30 (49.2%)
Community Organization
23
5 (21.7%)
Navigator
35
11 (31.4%)
Total
759
104 (13.7%)
Hispanic, while a larger minority were White nonHispanic (19.5%, n ¼ 16) and Hispanic (6.1% n ¼ 5). Table 1 shows referral outcomes for those referred by gender and by prior knowledge of PrEP. Overall those with prior knowledge of PrEP were significantly more likely to complete the process of screening for PrEP. While fewer than a third (29.6%) of those with no prior knowledge of PrEP were screened, more than two thirds (70.4%) of those with prior knowledge went on to screen for PrEP (X2 p < 0.0001). This pattern held true for women (75.0% with prior knowledge, 34.3% without, Fisher p ¼ 0.01) and men (66.7% with prior knowledge, 26.3% without, X2 p < 0.0001). Among men 34.8% had heard of PrEP while for women only 15.2% had heard of PrEP prior to their referral (X2 p-value<0.001). The referral source was known for 759 referrals (96.8% reporting). As shown in Table 2, the primary referral source was the health center HIV Rapid Testers. More than three quarters (81.3%) of all referrals were from the Rapid Testers. While only 7.1% of Rapid Tester referrals proceeded to initiate PrEP, these collectively constituted a substantial portion (40.0%) of PrEP initiators. The percentage of Rapid Tester referrals initiating PrEP increased at month 9 of the study when a PrEP team member was located at the busiest testing site one day a week. This increase brought the Rapid Testing referrals who went on to initiate PrEP from 5.6% at 8 months, to 7.1% in this analysis (17 months). The greatest ratios of initiation: referral were observed for clinician and self/peer/partner referrals. Of the 61 persons referred by clinicians, 30 (49.2%) went on to initiate PrEP, and of the 23 self, peer and partner referrals, more than half (60.9%, n ¼ 14) initiated PrEP. Overall, 14.0% of individuals (8.8% of women and 17.3% of men, p < 0.05) referred for PrEP completed the engagement process and initiated PrEP.
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Discussion The United States FDA was the first national regulatory body to approve TDF/FTC for PrEP,6 placing the US in the position of world leader in real world PrEP implementation. National uptake to date suggests that current strategies for implementation have had differential success across racial, ethnic and gender lines, with some communities at highest risk accessing PrEP the least. In a largely Black clinic population in Philadelphia, 61.4% of men and 54.8% of women expressed an interest in PrEP.21 Yet this high level of interest may not necessarily translate into utilization, as suggested by Rolle et al in an observational prospective study of young Black MSM in Atlanta.22 In this latter study only 35% from this high-risk cohort initiated PrEP despite high levels of interest.22 Although a large internet study of MSM noted no difference in reported PrEP utilization by race, authors cautioned that the small number of Black MSM in the study may limit the power to detect differences by race.23 In the Deep South, where Black communities may be the most impacted by HIV, limited PrEP uptake among Black men and women, including Black MSM, is reported.24 This current study provides some data on factors impeding and those facilitating engagement in PrEP for a majority Black cohort in urban US. It is important to note that among presented models of PrEP engagement is sameday PrEP initiation,25 which would theoretically eliminate the drop-off across the engagement cascade. For many settings this same-day start approach may not be feasible, hence these data are of relevance to the discourse on PrEP engagement, and to the discussion of strategies for engagement of racial minorities as well as for women. Gender. In this study initiation rates were higher for men than for women. The higher rates in men were driven in part by greater levels of prior knowledge of PrEP, a factor we found to be highly associated with PrEP initiation. Low levels of PrEP awareness among women have been previously documented. In a group of 39 women participating in focus groups in Washington DC, only 5 had heard of PrEP.26 Media campaigns and other strategies to improve awareness of PrEP especially and specifically in Black communities is a necessary part of increasing access to PrEP. Variations in prior knowledge of PrEP may not fully explain the gender difference in initiation rates. Chisquared tests performed at each stage of the engagement model showed gender differences of statistical significance in scheduling screening appointments. This difference in scheduling screening appointments is explained in part by differences in insurance status. Insured patients reluctant to change their PCP to the health center were not eligible to
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receive PrEP or other services at said health center, paradoxically resulting in a smaller percentage of the insured proceeding to PrEP initiation within our system. Women were statistically more likely to be insured, accounting in part for the gender difference in scheduling appointments. Hence at facilities without the requirement that patients switch their PCP, the gender difference in PrEP initiation rates may be smaller. Indeed, lack of insurance has been reported as a documented barrier to PrEP access in other settings,27 highlighting the nuances of the impact of lack of insurance on access to PrEP by site. For those scheduling appointments, there was no gender difference in screening completion. However, among those completing screening appointments, women were less likely to proceed with PrEP initiation although they were not less likely to be medically eligible. Race and ethnicity. Initiation rates also differed by race and ethnicity. Non-Hispanic Blacks constituted a smaller percentage of initiators than referrals. Conversely, Hispanics and non-Hispanic Whites represented a larger percentage of initiators than referrals. Essentially among a group of high-risk patients referred for PrEP, non-Hispanic Blacks were the least likely to proceed through the engagement process to begin PrEP. This finding has been reported in previous research. Katz et al noted that among MSM in Seattle, levels of engagement were substantially lower for Asian and Black MSM compared to White MSM (21% and 22% respectively compared with 40%).28 The lower rate of completing the process of accessing PrEP for Blacks, a group highly impacted by HIV, in a setting that eliminated lack of health insurance as a barrier, is cause for concern. Research shows that engagement of Black MSM in a client-centered model with care coordination is feasible.29 Further studies such as this are urgently needed to examine successful models, and to evaluate reasons and remedies for differential access by race. Referral source. Table 2 shows the percentage starting PrEP by referral source. The least efficient referral source was the HIV Rapid Testers, 7.1% of their 617 referrals going on to initiate PrEP. Having a member of the PrEP team at the busiest Rapid Testing site one day a week improved the percentage of referred patients from that site who proceeded to screening appointments. HIV testing offers a unique opportunity for the discussion of PrEP, and this discussion may be most impactful at the time of testing. Having trained staff on-site to discuss PrEP as a part of the testing process helps to capitalize on this opportunity. While the percentage of Rapid Tester referrals beginning PrEP was low, they were an essential referral source partly because they reached a population otherwise unengaged in the health care system, partly because the
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sheer volume of referrals was such that even a small percentage constituted a substantial portion of initiators, and also because the nature of their role makes them a natural fit for initiating a discussion about HIV risk and PrEP. Self/peer/partner referrals yielded the highest proportion of initiators, followed by clinician referrals. Patients seeking PrEP as a result of self/peer/partner referrals were a select group highly motivated to seek out PrEP and hence had high rates of completing the access process. Strategies to disseminate information about PrEP directly to communities, and to encourage PrEP referrals within social and sexual networks, will be important in engaging communities at risk in PrEP care. Those referred by a clinician were able to have their clinical questions answered, and begin the process of evaluation for medical eligibility during the same visit, which facilitated their initiation. Clinician recommendations may also have been considered more seriously by patients than recommendations of others, given existing relationships of trust between clinician and patient. Encouraging clinicians to initiate conversations about PrEP with patients is a potentially important component of improving access. PrEP awareness. Participants who were aware of PrEP were substantially more likely to complete the PrEP access process. PrEP awareness campaigns should target all groups at elevated risk for HIV, including communities of color.
IMPLICATIONS In this study, the low percentage of high-risk referred patients who completed the access process and initiated PrEP suggests a need for support and facilitation at each step of the PrEP engagement cascade, particularly for populations with steeper fall-off such as those who have never heard of PrEP, non-Hispanic Blacks, and women. Continuing to monitor the impact of insurance in different settings is important as the insurance landscape undergoes shifts. The domestic HIV epidemic impacts non-Hispanic Blacks to a greater degree than other groups. It is critical that the necessary effort be invested in engaging this community despite a potentially greater degree of difficulty. Should we fail to improve PrEP utilization among racial/ethnic minorities, existing disparities in HIV prevalence stand to grow.
high risk heterosexuals: subgroup analyses from the Partners PrEP Study. AIDS, 27(13), 2155e2160. 3. Grant, R. M., Lama, J. R., Anderson, P. L., et al. (2010). Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med, 363(27), 2587e2599. 4. Choopanya, K., Martin, M., Suntharasamai, P., et al. (2013). Antiretroviral prophylaxis for HIV infection in injecting drug users in Bangkok, Thailand (the Bangkok Tenofovir Study): a randomised, double-blind, placebo-controlled phase 3 trial. Lancet, 381(9883), 2083e2090. 5. Grohskopf, L. A., Chillag, K. L., Gvetadze, R., et al. (2013). Randomized trial of clinical safety of daily oral tenofovir disoproxil fumarate among HIV-uninfected men who have sex with men in the United States. J Acquir Immune Defic Syndr, 64(1), 79e86. 6. United States Food and Drug Administration (FDA). (2012). FDA Approves First Drug for Reducing the Risk of Sexually Acquired HIV Infection. Washington, DC http://www.fda.gov/NewsEvents/ Newsroom/PressAnnouncements/ucm312210.htm.
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