Pre-exposure prophylaxis (PrEP) with daily oral tenofovir/emtricitabine is effective for HIV prevention.1 PrEP has been shown to be acceptable to men who have sex with men (MSM) who are at increased risk of HIV infection, with high rates of PrEP uptake across all subgroups when offered as part of open-label studies and demonstration projects.2,3 Administering PrEP in a real-world setting requires longitudinal follow-up for HIV testing, safety monitoring, counseling, and drug prescribing.4 Retention in care among those taking PrEP medication is essential for continued access to medication, reinforcement of adherence, HIV and STI testing and treatment, and has been a challenge in some real-world settings.5,6 Patterns of retention in PrEP care may vary; 3 clinically important categorizations of these patterns include those who are interested in PrEP but do not follow up beyond the initiating visits, those who continue to follow up but miss 1 or more visits, resulting in less than complete coverage with PrEP medication, and those who follow up regularly as scheduled. These patterns of retention may have different implications for safety and future engagement. Understanding individual- and community-level characteristics of PrEP users who exhibit various patterns of retention in PrEP care, may allow tailored interventions to improve retention. In this study, we sought to describe the patterns of retention in the multi-site United States National Institutes of Health PrEP Demonstration Project (The Demo Project) and to identify baseline and early characteristics that are associated with these 3 patterns of retention in PrEP care.
The Demo Project was a multi-site open-label demonstration project that enrolled 557 MSM and transgender women with increased risk of HIV infection from 2 municipal sexually transmitted disease clinics (in San Francisco and Miami) and a community health center (in Washington, DC). Three individuals with detectable HIV-1 nucleic acid amplification at the first medication dispensation visit after nonreactive rapid tests were excluded from the analysis. One individual who experienced HIV seroconversion after loss to follow-up from the study was included in the analysis. Baseline characteristics and primary outcomes of the project have been previously reported.2,7 Baseline screening evaluation was conducted to assess eligibility, and eligible individuals who elected to enroll in the project had a separate enrollment visit 1–2 weeks after the screening visit at which medication was dispensed. Scheduled follow-up visits were at 4-, 12-, 24-, 36-, 48-, and 52-weeks postenrollment. PrEP medication was dispensed directly to the participants at each follow-up visit, with sufficient medication for daily dosing through the scheduling window for the next scheduled visit as follows: at the enrollment visit, one 30-pill bottle of medication was dispensed; at the 4-week visit, 2 bottles were dispensed; and at the 12-, 24- and 36-week visits, 3 bottles were dispensed. No medication was dispensed at the 48- or 52-week visits. Participants who had delayed or missed visits were dispensed the number of bottles required to provide daily medication until the next scheduled visit and lapses were noted. Assessment included pill counts, surveys, biological samples, health screenings including review for adverse events, physical examination, and HIV and STI testing. Participants were encouraged to continue to attend appointments even if they had temporarily or permanently discontinued PrEP medication.
Dried blood spot (DBS) samples for tenofovir diphosphate (TFV-DP) levels were collected at all scheduled follow-up visits and any visit in which PrEP medication was stopped. Samples were processed for 100 randomly selected participants from each site, as well as for all black and transgender participants because these groups were underrepresented in the overall sample. DBS samples were analyzed for TFV-DP levels as previously described.3,7,8
Participants were contacted by telephone in advance of all scheduled study visits. Contact was attempted at least 3 times with each participant who missed a scheduled study visit. All participants were required to provide alternate contact information at study enrollment; for participants not responding after 3 attempts, contact through the alternative contact was attempted. These procedures were repeated each time a study visit time window opened. All contact and retention procedures were standardized across sites. Ongoing communication between study sites and comparison of contact logs occurred throughout the study to ensure uniformity in retention procedures.
Questionnaires were verbally administered by study personnel in English or Spanish depending on the participant's preference. Questions addressed demographics, employment, educational attainment, income, financial security (a response other than “never” to the question “in the past 6 months how often has there not been enough money in the household for rent, food, or utilities”), sexual behavior including number of partners, HIV status of partners, and reported condom use, current substance use, PrEP awareness, depression [as measured by a Patient Health Questionnaire-2 (PHQ-2) screening instrument score of greater than 2], and HIV-risk perception. Risk perception was assessed by asking, “if you were not receiving PrEP, what is the likelihood that you would acquire HIV within the next year,” with an answer scale of 0–100. Answers were categorized as “low” (0–49), “medium” (50), or “high” (51–100). The decision to categorize “medium” with a single value response was made due to a large spike in responses at the value “50.”
Patterns of Retention
After visual examinations of the patterns of follow-up, 3 categories were created. We defined the early loss to follow-up (ELTF) group (N = 61) as those completing enrollment procedures and receiving at least a 30-day supply of medication, but not attending the 12-week scheduled visit or any subsequent visits. The intermittent group (N = 127) included those participants completing enrollment and 1 or more study visits at 12 week or later, but missing or delaying at least 1 follow-up visit during the study at which medication was to be dispensed, resulting in at least 1 month with medication coverage for <50% of days and therefore not considered to have continuous coverage with PrEP medication throughout the study period. Finally, the retained group (N = 366) included those enrolled and attending all scheduled follow-up visits at which medication was dispensed. Because no medication was dispensed at the 48-week and 52-week visits, participants who completed all other visits were included in the retained category regardless of the attendance at these visits. Two participants who were enrolled in the study and received medication at enrollment but did not return for any subsequent visits until the 48-week visit (at which no medication was dispensed) were included in the ELTF group.
For each retention group, baseline and enrollment survey responses, demographics, and clinical characteristics were tabulated. Initially, each potential predictor was assessed for relationships with the 3 retention groups using multinomial logistic regression adjusting for site only. Using this model, we calculated odds ratios for ELTF vs. retained and intermittent vs. retained groups. Because of high multicollinearity of measures within different domains (eg, demographics, behaviors), we built our multivariate model in stages by domain. In the first stage, predictors were divided into demographic and behavioral domains, and a multivariable model for each was created by adding in all variables in which P < 0.05 in the initial models. In the second stage, these 2 models were combined into a single model by including those predictors from these 2 intermediate models with P < 0.05. The 3 odds ratios were also calculated for each of the variables retained in the final multivariable model.
DBS samples were analyzed separately because they were available only on a subset of individuals. For DBS samples, protective levels of TFV-DP were defined as >700 fmol/punch based on the available modeling data.9 Levels were scored as protective or not protective at each visit where levels were obtained, and the percentage of samples with protective levels was reported for each retention group and compared across groups using a Wilcoxon test.
Overall, 366/554 (66.1%) of the enrolled participants in the Demo Project were retained for all study visits, 127/554 (22.9%) had intermittent retention, and 61/554 (11.0%) had early loss to follow-up (ELTF). Demographic and baseline characteristics of each group with χ2 assessment of differences in characteristics between groups are described in Table 1 (additional baseline characteristics are described in Table 1, Supplemental Digital Content, http://links.lww.com/QAI/B165).
Factors Associated With Retention in Bivariate Analysis
Compared with the San Francisco and Washington, D.C. sites, the prevalence of ELTF was higher at the Miami site (Table 2). Enrollment at the Miami site was significantly associated with both ELTF [vs. complete retention aOR 7.69; confidence interval (CI): 4.17 to 14.28] and intermittent retention (vs. complete retention aOR 2.63; CI: 1.64 to 4.17) compared with the San Francisco site and with the Washington, D.C. site for ELTF (vs. complete retention aOR 7.69; CI: 2.94 to 20.00) and intermittent retention (vs. complete retention aOR 3.22; CI: 1.72 to 6.25). There were no significant differences in retention between the Washington, D.C. and San Francisco sites. All further comparisons are adjusted for site.
Younger age and unstable housing were each significant predictors of both ELTF and intermittent retention compared with full retention. Black, disabled or unemployed status, annual income less than $20,000, financial insecurity, lack of previous PrEP awareness, reporting sex work (giving or receiving money or other things for sex), and lack of primary care physician were significantly associated with ELTF compared with full retention in the bivariate analysis (Table 2). Drug use was not significantly associated with retention categories except for use of erectile dysfunction medication, which was protective against ELTF compared with full retention (aOR 0.29; CI: 0.12 to 0.71). Reporting a lower number of known HIV-seropositive sexual partners was protective against ELTF compared with full retention (aOR 0.34; CI: 0.12 to 0.99) as was a lower number of known HIV-seronegative sexual partners (aOR 0.49; CI: 0.27 to 0.88).
Multivariate-Adjusted Factors Associated With Patterns of Retention
The multivariate model included the following variables in relation to retention categories: site, age, race, sex work, previous PrEP awareness, reported number of known HIV-positive partners, and employment status (Table 3). All comparisons reported in this section are adjusted for all the other variables in the model.
Factors Associated With Both ELTF and Intermittent Retention
In the multivariable model, the Miami site when compared with the San Francisco site was associated with ELTF rather than full retention (aOR 2.84; CI: 1.24 to 6.47) and also with intermittent rather than full retention (aOR 2.70; CI: 1.43 to 5.11). Decrease in age by 10 years was significantly associated with both ELTF (aOR 1.80; CI: 1.26 to 2.57) and intermittent retention (aOR 1.47; CI: 1.67 to 1.84) compared with full retention (Table 2).
Factors Associated With ELTF but Not Intermittent Retention
Black race was associated with ELTF compared with full retention (aOR 3.32; CI: 1.09 to 10.16). Lack of PrEP awareness before study enrollment was associated with ELTF (aOR 2.01; CI: 1.01 to 3.96 for ELTF vs. full retention). Being disabled or unemployed vs. working part- or full-time was associated with ELTF compared with full retention (aOR 2.53; CI: 1.27 to 5.05). Participating in sex work was also associated with ELTF compared with full retention (aOR 4.67; CI: 1.49 to 14.58).
Sexually transmitted infections were present at baseline for 23/61 (37.7%) of the ELTF group, 81/366 (22.1%) of the retained group, and 39/127 (30.7%) of the intermittent group; the difference was significant (χ2 = 8.68; P = 0.013). When adjusted for reason for baseline visit (“to get PrEP” vs. “other”), this difference was no longer significant.
There were no significant differences between the retention groups in total reported adverse events, adverse events attributed by participants to PrEP medication, or gastrointestinal adverse events up to the 4-week visit. There were no differences in social harms or social benefits reported up to the 4-week visit across groups (data not shown).
Patterns of Drug Detection
Levels of TFV-DP were most consistently protective among those in the retained group, with 257/314 (81.8%) having protective levels for all DBS samples obtained compared with 50/113 (44.2%) and 8/24 (33.3%) for the intermittent and ELTF groups, respectively. Of those who had blood drawn for TFV-DP levels in DBS samples at week 4, 174/191 (91.1%) were protective (>700 fmol/punch) for those subsequently retained for all visits compared with 10/24 (41.6%) for those who were in the ELTF group and 56/78 (71.8%) for those in the intermittent group (Fig. 1).
Most participants in the PrEP Demo Project were retained in care throughout the study period. For those not fully retained, 2 patterns were examined: early loss before the 12-week visit and intermittent retention throughout the study with gaps in PrEP medication coverage. These patterns may be driven by different factors. Individuals who dropped out of PrEP care early in the process may have made an early decision to terminate PrEP, may never have been committed to PrEP as a prevention strategy, may have been discouraged by lack of social support, or may have structural or logistical constraints that make PrEP care difficult or a lack of previous preparation for participation in an intervention that requires longitudinal engagement. Intermittent care, by contrast, indicates at least some continued interest in PrEP. Less-than-complete engagement may be a marker of fluctuating risk/risk perception or may represent difficulty attending appointments because of scheduling, transportation, or other logistics.
These patterns of care may also have different implications for safety, monitoring, and protection from development of HIV Infection. For example, individuals who are intermittently engaged in care may be taking medication less than daily, leading to drug levels below those expected to confer protection (and theoretically placing at risk of development of resistance, should HIV infection occur). Those both intermittently engaged in care and those experiencing ELTF would have experienced periods of time without medication coverage, potentially leading to HIV infection risk and less frequent HIV and STI testing.
Although decision making about PrEP use is complex and may depend on fluctuations in risk perception, changes in partners, and personal decision making regarding prevention choices, these choices would ideally be made with appropriate monitoring and guidance from an experienced PrEP provider. Although risk perception has been previously associated with PrEP uptake and maintenance,10,11 we did not find an association between reported baseline risk perception and pattern of retention in our study cohort. We cannot rule out a change in risk perception leading to early discontinuation among some participants. However, the short time frame between initiation and loss for the ELTF group would argue against perceived change in risk as a driver of loss from this group.
Study site and age were strong predictors of incomplete retention including ELTF, as well as intermittent retention, in our cohort. Community support and individual preparedness for embarking on PrEP care have been demonstrated in previous qualitative analyses to be important to PrEP adherence12–14 and are likely to also impact retention. Qualitative data from retained and nonretained PrEP recipients in Mississippi reinforce the importance of social and relationship dynamics and stigma in decision making regarding PrEP continuation.6 As protocols for retention were standardized across sites, these observed differences might reflect differences in unmeasured variables such as stigma, social support, and community PrEP awareness and acceptability in the communities enrolling participants in the Demo Project.
Younger age was associated with ELTF and intermittent follow-up in our study; this is consistent with findings from the ATN 110 trial indicating that PrEP adherence declined among youth when follow-up intervals increased15 and suggests that maintenance of close follow-up, as well as additional counseling support, may be beneficial for younger PrEP patients.
Black participants in our study cohort were more likely than white participants to experience ELTF than either full study retention or intermittent retention. This is consistent with previously published data from 3 PrEP-prescribing clinics, indicating decreased retention in PrEP care at 3 months but not at 6 months for black clients compared with white clients.5 As black gay and bisexual men are the demographic group most impacted by HIV in the United States.,16 this finding is concerning and suggests the need for additional support early in PrEP engagement for black MSM. Other studies suggest that factors such as stigma in social networks, internalized homophobia, and lack of support from partners and community may have critical impact on PrEP engagement including uptake, adherence, and retention among black MSM in the United States.5,17 Strategies such as peer navigation and counseling to provide intensive support in the first 3 months of care may help alleviate these observed disparities in retention in PrEP care.
PrEP awareness before study engagement was also associated with increased retention and protective against ELTF. As the Demo Project took place soon after FDA approval of TDF/FTC for PrEP, previous awareness may in some cases have been a proxy for highly motivated early adopters who actively sought PrEP in an environment where it was not widely available. In addition, drawing on the Stages of Change/Transtheoretical model, as has been applied to PrEP and termed the PrEP Motivational Cascade,18 individuals who learned about PrEP only at the time of study screening may not have had time to move through stages of contemplation and preparation, coming into PrEP care with ambivalence or less motivation/commitment to the process compared with those who were aware of PrEP before screening. Although it is difficult to know what triggered early loss from the study, continued longitudinal follow-up with opportunities to address concerns and provide for re-engagement at a later time may result in re-engagement of some of the participants who were initially lost to follow-up.
Employment status was a predictor of ELTF in our multivariate model. We theorize that employment status may be a marker of more consistency in daily routine and organization, as well as legal status in the United States., factors that may also contribute to an individual's ability to stay in medical care and attend study visits. The role of individual-level economics in PrEP decision making is likely complex and includes other unmeasured variables such as availability of transportation and opportunity costs related to attending PrEP study visits. Additional innovation to increase flexible and convenient access to PrEP may facilitate engagement with individuals with irregular or inconsistent schedules who may otherwise be lost from PrEP care. Exchanging sex for money or other goods was also a predictor of ELTF, again reinforcing the concern that those individuals who are most in need of prevention strategies may also have difficulty following up longitudinally as is currently required for PrEP care. Sex work has been associated with substance use, mental health issues, and childhood sexual trauma,19 as well as decreased access to health care.20 A holistic approach to PrEP care including mental health interventions may be needed to facilitate retention in care for this vulnerable and stigmatized population. Innovative strategies including nontraditional placement in time and space for PrEP care (such as community-based clinics with extended hours, mobile clinics, and PrEP evaluation via telehealth) may allow those with alternative schedules and other constraints to engage successfully in care.
DBS drug levels for PrEP medication presented a complex picture. Early (at 4 weeks) drug levels strongly correlated with future retention. However, we noted a group of participants who had inconsistent retention in PrEP care but demonstrated adherence to taking PrEP during the time that they were in the study. Logistical difficulties may have made the study follow-up difficult despite intentions to take PrEP, or self-selection for stopping PrEP (and not coming to subsequent study visits) may have occurred because of changes in risk behavior, risk perception, or other factors influencing perceived need or desire for PrEP. Although early objective measures of adherence such as drug levels could allow intervention for those not taking PrEP medication consistently, additional evaluation for risk of loss from PrEP care may also be required. A careful appraisal of the risk of loss to follow-up at the first PrEP follow-up visit and consideration of more close follow-up intervals (in person or remotely) for those with risk of loss from care may be beneficial to increasing retention.
Participants in the ELTF group reported sexual behavior conferring significant risk of HIV infection and had high rates of baseline STIs equal to those retained in the study when adjusted for reason for initial visit, indicating an urgent need for prevention services among those lost to follow-up. Interventions are needed for those with early loss from PrEP care to encourage re-engagement with PrEP or, if PrEP is not desired, to facilitate access to other prevention services such as condoms, appropriate STI and HIV testing, and prompt STI treatment as needed.
Our study has several limitations. The analyses in this study were exploratory; nevertheless, they provide important initial estimates of the factors to be addressed in future research on PrEP adherence and continuation over time. The environment and support provided through a demonstration project are different from that offered in clinical practice; in particular, participants were provided with a stipend for participation and were directly dispensed medication at the study site. In addition, those who elected to temporarily or permanently discontinue PrEP medication were encouraged to continue follow-up and received HIV and STI testing quarterly. For these reasons, the retention described may be considered a “best case scenario” for the time frame of the study. The study environment, however, could also negatively and disproportionately influence engagement among groups with historical mistrust of medical research, and the longer visits required because of study procedures could also have influenced retention. Retention differed significantly by site, and baseline characteristics of participants also differed significantly by site, making cross-site comparisons challenging. Although we cannot rule out an unintended difference in site retention practices, attempts were made at all sites to standardize these procedures. The small number of black and transgender participants in the Demo Project precludes more nuanced conclusions about these subgroups based on our data. Further investigation of potential risk and protective factors for retention in PrEP care for these important groups are needed. Decision making regarding retention in PrEP care may be in some cases linked to reduction in sexual risk or adoption of alternative prevention strategies that reduce the need for PrEP. We were not able to successfully query sufficient participants who were lost from the study to determine reasons for loss. Although we noted that baseline risk was similarly high in all categories of retention in our study, we do not have detailed follow-up risk information for those who were lost to follow-up or intermittently retained in the study. Furthermore, the intermittently retained participants, while all having at least some missed days of PrEP medication, are a heterogeneous group with a wide range of patterns of missed or delayed visits, limiting closer analysis of this group.
In summary, we found that retention in the PrEP Demo Project was influenced by site, but also varied by factors such as age, race, employment status, and previous PrEP awareness. Risk factors, as measured by partner number and STIs, were high in participants who were lost from care, as well as those who were retained. Overall, our data reinforce previous observations21–23 that effective PrEP delivery remains a challenge to high-priority geographic areas (eg, the Southern United States), black MSM, and to individuals with low SES even within a highly favorable environment such as a demonstration project in which all visits, laboratory tests, and medication were provided free of charge, and participants received a stipend for participation. Addressing not only PrEP initiation but also in retention and persistence in PrEP care is essential to avoid perpetuation and worsening of racial, socioeconomic, and geographic disparities in the HIV epidemic.21,24 Early assessment of risk of loss from care and consideration of interventions to improve retention by enhancing education, motivation, and social/psychological support during early PrEP visits may enhance continuation in PrEP care. Key populations, such as black MSM and younger adults, are disproportionately lost in the first 12 weeks of PrEP care. Youth additionally require longitudinal support to avoid intermittent engagement in PrEP care. Focused interventions to retain these priority populations in PrEP care once initially engaged are urgently needed.
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