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Prevention Research

HPTN 067/ADAPT: Correlates of Sex-Related Pre-exposure Prophylaxis Adherence, Thai Men Who Have Sex With Men, and Transgender Women, 2012–2013

Holtz, Timothy H. MD, MPHa,b; Chitwarakorn, Anupong MDc; Hughes, James P. PhDd,e; Curlin, Marcel E. MDa,b,f; Varangrat, Anchalee MAa; Li, Maoji MSe; Amico, K. Rivet PhDg; Mock, Philip A. MAppStatsa; Grant, Robert M. MDh; the Thai HPTN 067/ADAPT Study Team

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: October 1, 2019 - Volume 82 - Issue 2 - p e18-e26
doi: 10.1097/QAI.0000000000002131



Oral pre-exposure prophylaxis (PrEP) is a highly effective method of HIV prevention, particularly for men who have sex with men (MSM). The U.S. Food and Drug Administration and U.S. Centers for Disease Control and Prevention (CDC) based the U.S. Health and Human Services 2014 recommendation of daily emtricitabine/tenofovir disoproxil fumarate (FTC/TDF) PrEP for HIV prevention solely on the results of the IPrEx study.1 More recently, however, the Ipergay trial2 and follow-up extension study3 demonstrated effectiveness of intermittent (also known as “on demand”) dosing consisting of a double FTC/TDF dose 2–24 hours before sex and an additional FTC/TDF dose on each of the 2 days after sex, a dosing schedule based on findings from animal models.4 The European AIDS Clinical Society currently recommends either daily dosing or on-demand dosing before and after sex.5

PrEP effectiveness requires a minimum threshold of medication use during periods of possible exposure to HIV. Because a phase 3 efficacy or equivalency trial of on-demand dosing of FTC/TDF PrEP is unlikely to be conducted among MSM or transgender women (TGW) in the near future; understanding the factors associated with high adherence among MSM and TGW on daily and nondaily dosing will be important for the future use of this known effective HIV prevention tool. In the first 2 placebo-controlled PrEP studies conducted including event-driven dosing arms, different measurements provided divergent estimates of adherence.6–8 Among MSM, studies of predictors of intention to take PrEP,9 acceptability and interest in PrEP,10,11 willingness to take PrEP,12–14 and attitudes toward PrEP uptake15 have been conducted, but characteristics associated with actual sex-related PrEP adherence among MSM using daily versus nondaily PrEP dosing remain unknown.

Adapting PrEP regimens to match infrequent or episodic sexual exposure could increase coverage during periods of risk while minimizing medication costs and side effects. Numerous demographic, social, and behavioral factors have been shown to substantially impede efforts to promote antiretroviral drug adherence in settings such as treatment for established infection.16 In the use of antiretroviral drugs for prevention, factors related to adherence to daily PrEP in a nonresearch setting have only recently been studied.17 Identifying correlates of sex-related PrEP adherence, whether through daily or nondaily dosing, could promote the reduction of HIV infection through the effective use of PrEP.

HPTN 067, the Alternative Dosing to Augment PrEP Pill Taking (ADAPT) study was a phase 2, randomized, open-label pharmacokinetic and behavioral equivalence study of daily and nondaily regimens of oral FTC/TDF PrEP among Thai MSM and TGW (Bangkok), US MSM (New York City),18 and in South African heterosexual women (Cape Town), completed in 2014.19 The primary outcomes in the HPTN 067/ADAPT trial among MSM showed that daily dosing increased coverage and protective drug concentrations in the New York City cohort, whereas in the Bangkok cohort both daily dosing and nondaily dosing resulted in: (1) high coverage (sex-related PrEP adherence) of sex events by pre-exposure and postexposure dosing; and (2) protective drug concentrations in blood consistent with use of ≥2 tablets per week in >95% of visits when sex was reported in the previous week. In this analysis we sought to identify correlates of adherence to PrEP among participants from the Silom Community Clinic site, Bangkok, Thailand, with New York City results analyzed separately.



We enrolled MSM and TGW into HPTN 067 at our community clinic and clinical research site. Participants were randomly assigned to daily or nondaily dosing of open-label oral TDF/FTC, with a primary objective to test the hypothesis that nondaily provides equivalent coverage of sex events (hereafter labeled “sex-related PrEP adherence”) with pre and postsex PrEP dosing compared with daily dosing. We used multiple methods to measure PrEP use in relationship to sex events.

Eligible MSM and TGW included those who met criteria for enrollment: male sex at birth, HIV-antibody negative, age ≥18 years old, normal renal function, hepatitis B surface antigen negative, literate in Thai, able to provide written consent, reported anal or neovaginal sex with a man in the past 6 months, and 1 of 4 major risk factors for HIV acquisition in the past 6 months (sex with >1 man or transgender woman; history of an acute STI; sex in exchange for money, goods, or favors; intercourse without a condom with an HIV-infected partner or partner of unknown HIV status).18 Participants in our Bangkok clinical research site were required to be immune to hepatitis B virus (HBV) either from a previous infection or vaccination; hepatitis B vaccination was provided as part of the study. Exclusion criteria included diagnosed HIV infection or symptoms of acute HIV, use of nephrogenic drugs, proteinuria or glycosuria, low serum phosphate, and recent postexposure prophylaxis or PrEP use.

Randomization and Dosing

Participants began with a 6-week directly observed therapy (DOT) lead-in phase, with 5 observed once-weekly DOT TDF/FTC doses followed by 1 week without dosing to determine individual steady-state pharmacokinetics. After this 1-week hiatus and blood draw, they were randomized 1:1:1 to one of 3 self-administered PrEP dosing strategies for 24 weeks. Participants in the daily arm were instructed to take one tablet once a day regardless of sexual activity. Time-driven arm participants received a recommendation to take one tablet twice a week, 3–4 days apart, regardless of sexual activity, in addition to one tablet postexposure within 2 hours after any penile intromission regardless of condom use. Event-driven arm participants received a recommendation to take one tablet between 24 and 48 hours before sexual intercourse, and a second postexposure dose within 2 hours after a sexual event. In addition, participants in all 3 arms were advised to take a dose if they thought they had missed a scheduled or event-driven dose, provided they took no more than 2 doses per day, and no more than 7 doses per week. Investigators, staff, and participants were not blinded to study arm assignment, but laboratory investigators were. Participants who acquired HIV infection during the study period were told to discontinue dosing and were followed until study closure and referred for poststudy care.

Data Collection

Study visit schedule, medication dispensation, counseling, and laboratory sampling procedures have been previously described.18 All participants received a real-time electronic drug monitoring (EDM) dispensing device (Wisepill, Somerset West, South Africa) at enrollment. Participants were given vitamin tablets during the 6-week lead-in phase to become familiar with the device and “opening events.” Participants were interviewed at screening, and were contacted weekly to obtain self-reported information on adherence and behavioral data by interviewers who were separate from the clinical team. Interviewers were trained to ask about EDM first, then solicit information regarding sexual events, first asking about the number of days sex occurred in the previous week, then reviewing sex events on a day-by-day basis, collecting detailed information on each event. During weekly interviews, phone interviewers used real-time EDM data to collect dates and times of sex events and PrEP use, and electronically recorded “opening events” were reconciled with reported pill taking and harmonized for date and time. Sexual events were queried regarding date, time, type of sex, condom use, and partner serostatus, and were dependent on self-report. The results of these EDM-guided weekly interviews were the basis for assessing sex-related PrEP adherence.

In addition, participants completed a computer-assisted self-interview at the time of screening, and at 6, 18, and 30 weeks, relating to attitudes and behaviors in the previous 12 weeks. The computer-assisted self-interview contained questions about alcohol and substance use, sexual behavior and frequency, HIV vulnerability, and barriers/facilitators of PrEP use. We use the Alcohol Use Disorders Identification Test (AUDIT) developed by the World Health Organization, a simple ten-item questionnaire for hazardous and harmful alcohol consumption and alcohol-related problems, and stratified scores into low (0–6), moderate (7–12), and high (≥13) alcohol use.20 Questions are sensitive to high-risk drinking, and are divided between consumption patterns and binging, psychological and/or physical dependence, and potential harm to physical and/or mental well-being. We also incorporated the Center for Epidemiological Studies-Depression measure, originally published by Radloff in 1977.21 It is a standardized tool that rates how often over the past week persons experienced symptoms associated with depression, such as restless sleep, poor appetite, and social isolation.

Further information about medication dispensation, counseling, and monitoring can be found in previous publications and supplementary material,

Laboratory Procedures

Testing for HIV, HBV, renal, and liver function were performed at screening, and HIV testing was repeated at weeks 4, 10, 18, and 30. Two HIV rapid tests were performed in parallel: Oraquick Advance HIV-1/2 Antibody Test (Orasure Technologies, Inc., Bethlehem, PA) and Determine HIV-1/2 Ag/Ab Combo test (Alere Medical, Ltd., Chiba, Japan). Individuals with one or more positive screening tests at enrollment were ineligible for participation, and underwent confirmatory testing. Enrolled participants with one or both screening tests positive during follow-up also underwent confirmatory testing, using an assay based on nucleic acid amplification (Aptima HIV-1 Qualitative RNA test; Hologic, Inc., San Diego, CA). Blood was collected at each visit, and plasma and peripheral blood mononuclear cell lysate were collected, prepared, and stored.

Statistical Analysis

The primary outcome was sex-related PrEP adherence. We defined a sexual event as anal or neovaginal intercourse (insertive or receptive anal and/or neovaginal sex), not including oral sex events. Sex-related PrEP adherence was calculated per protocol as the proportion of sex events covered by PrEP use (at least one tablet taken within 4 days before sex and at least one tablet taken within 24 hours after sex) to total sex events based on electronic dose monitoring data corrected with weekly interviews that confirmed dose data and collected sex event details. The definition of sex-related PrEP adherence was identical in all randomization groups, and we used sex event as the unit of analysis.

We used medians to summarize quantitative measures and proportions for categorical measures. Because participants provided adherence data to multiple sexual events, giving rise to clustered data, we performed logistic regression analyses using generalized estimating equations with robust standard errors, clustered by participant to estimate the association between adherence and each potential correlate as measured at screening. Selected correlates were randomization arm, age, education, employment, alcohol and drug use characteristics, depression score, number of sex partners and events in the past 3 months, and whether participant reported any anal intercourse event without a condom in the last 3 months. All correlates were included in a multivariate model and were considered significant if P < 0.05.

We investigated the relationship between sex event frequency (outcome) and drinking frequency (AUDIT) at screening, using a negative binomial model with robust variance. Similarly, we examined the relationship between randomization arm and the self-reported number of sex events in the past 3 months, as measured at screening.



We screened 249 people between June 2012 and July 2013, and enrolled 193 (enrollment to screening ratio: 0.78); 56 were excluded from enrollment mainly because of abnormal transaminases (13/23.2%), positive rapid HIV testing (11/19.6%), nonimmunity to HBV (11/19.6%), and other reasons (21/37.5%) (Fig. 1). Among the 193 enrolled, 15 (7.8%) could not be randomized, including one because of a Thailand protocol deviation. Four participants were not randomized, because they had reactive/positive HIV tests. This included 2 who had false reactive HIV rapid tests during the DOT phase, one who had acute HIV infection at enrollment, and one who acquired HIV infection during the DOT phase. In total, we randomized 178 participants into one of 3 study arms. There were no seroconversions during the randomized follow-up phase of the study, and one participant withdrew consent. Retention through the end of the self-administered dosing phase was 97%.

Consort diagram for the HIV Prevention Trials Network (HPTN) 067/alternative dosing to augment PrEP pill taking (ADAPT) study in Bangkok, Thailand, 2012–2013. ALT, alanine aminotransferase; AST, aspartate aminotransferase; Ser Cr, serum creatinine.

Participant Characteristics

Among the 178 randomized participants, 2 (1.1%) identified as TGW, and the rest as cisgender men (Table 1). All participants were Thai, and the median age was 31. Most participants were unmarried (173/97.2%), had completed college (148/83.1%), and reported full-time employment (148/83.1%). At baseline, half of the population reported having 10 or more sex events in the past 3 months (through the weekly calls, participants recorded a median of 13 sex events during the 24-week self-administered phase). Sex without a condom (65/36.5%) and 5 or more sex partners (63/35.4%), both in the past 3 months, were commonly reported at screening.

Baseline Demographic and Behavioral Characteristics Among Participants Randomized in the HIV Prevention Trials Network (HPTN) 067 Study, Bangkok, Thailand (n = 178), 2012–2013

Substance use was common in the 3 arms, with 42 (23.6%) participants reporting drug use in the past 3 months. At screening, 15 (8.4%) reported use of stimulants, including 5 (2.8%) who also reported use of marijuana, and 3 (1.7%) who also reported use of opiates (noninjection). In addition, 27 (15.2%) reported primary use of drugs from pharmacologic groups such as nitric oxide, gamma hydroxybutyrate, heroin, methadone, ketamine, phencyclidine, mandrax, benzodiazepines, and erectile dysfunction drugs. AUDIT scores indicated moderate (7–12) alcohol use by 37 (20.8%) and high (≥13) alcohol use by 12 (6.7%) participants.

While investigating confounding factors, we found that the odds of having one more sex event was 18% higher in participants with a high AUDIT score (≥13) than those with moderate alcohol use (AUDIT 7–12), but the difference was not statistically significant [odds ratio (OR) 1.18, P = 0.64]. There was a nonsignificant trend toward more sex events with higher AUDIT. In contrast, there were statistically significantly fewer sex events reported in the participants randomized to the event-driven arm compared with the time-driven arm at screening (OR 0.60, P < 0.01), but not when compared with the daily arm (OR = 0.76, P = 0.09 at screening). Overall, there was a difference in the number of sex events by arm, with fewer sex events in the event-driven arm, that was not because of the intervention.

Sex-Related PrEP Adherence

Sex-related PrEP adherence was highest in the daily arm (85.3%, 1266/1485 events), but comparable to adherence in the time-driven dosing regimen (84.4%, 1129/1337 events, P = 0.79 versus daily), whereas adherence was slightly lower in the event-driven dosing arm (73.6%, 749/1018 events, P = 0.02 versus daily).

In univariate analysis, only age 26–35 years was significantly associated with higher sex-related PrEP adherence compared with age 18–25 years, whereas being randomized into the event-driven arm, having a higher number of reported sex events (13–80 over 3 months at screening), and use of stimulant drugs with or without other drugs were associated with lower sex-related PrEP adherence (Table 2). Sex-related PrEP adherence by those reporting stimulant use [74.2% (221/298)] was similar to those reporting other nonalcohol drug use [76.3% (670/878), P = 0.80], but lower than those reporting no substance use [84.6% (2253/2664), P = 0.04]. Moderate levels of alcohol use (AUDIT Score 7–12: P = 0.07), and high levels of alcohol use (AUDIT Score ≥13: P = 0.47), were not associated with sex-related PrEP adherence.

Univariate and Multivariable Model of Correlates of Sex-Related PrEP Adherence in the HIV Prevention Trials Network (HPTN) 067 Study, Bangkok, Thailand (n = 178), 2012–2013

Adjusting for covariates in a multivariable model, age 26–35 years [adjusted OR (aOR) 2.39, 95% confidence interval (CI) 1.46 to 3.92, P < 0.001] and age >35 years (aOR 1.82, 95% CI: 1.08 to 3.07, P = 0.02), completion of college (aOR 1.62, 95% CI: 1.01 to 2.58, P = 0.04), moderate levels of alcohol use (AUDIT Score 7–12: aOR 1.94, 95% CI: 1.29 to 2.93, P < 0.01), and high levels of alcohol use (AUDIT Score ≥13: aOR 2.44, 95% CI: 1.02 to 5.81, P = 0.04), were statistically significantly associated with higher sex-related PrEP adherence. Randomization to the event-driven arm (compared with daily aOR 0.54, 95% CI: 0.35 to 0.84, P < 0.01, compared with time-driven aOR 0.52, 95% CI: 0.33 to 0.81, P < 0.01), having a higher number of reported sex events (13–80 over 3 months at screening: aOR 0.54, 95% CI: 0.32 to 0.91, P = 0.02), and use of stimulant drugs (aOR 0.47, 95% CI: 0.25 to 0.90, P = 0.02) were significantly associated with lower sex-related PrEP adherence in the multivariable analysis (Table 2).

With the strength of association between use of AUDIT score and apparent higher coverage, we examined sex-related PrEP adherence for AUDIT scores stratified by use of stimulants and other illicit drugs. Although the sample sizes were small for stimulant users, we found no interaction between alcohol use, stimulant use, and adherence.


In this analysis of HPTN 067/ADAPT phase 2 clinical trial data of daily versus nondaily PrEP, Thai MSM and TGW study participants randomized to daily and time-driven arms overall achieved >84% sex-related PrEP adherence. In a multivariable model, we found that use of stimulants, age less than 26, lack of a college education, high sexual frequency in the past 3 months and randomization to event-driven use of PrEP were associated with lower sex-related PrEP adherence, whereas moderate and heavy alcohol use were unexpectedly associated with higher adherence.

Stimulant use (including amphetamine-type stimulants) was common in this clinical trial participant population, and has been cited as a growing problem among MSM and TGW populations worldwide.22 Stimulant use has been associated with high-risk sexual behavior in many studies including those among MSM,23 on HIV seroconversion,24 and with poor adherence to antiretroviral therapy (ART) among HIV-infected MSM,25,26 although the effect of stimulant use on PrEP adherence has been understudied. In the TAPIR multicenter PrEP study analyzing adherence using dried blood spots, post-trial observation phase (31%), predictors of higher adherence were those with less problematic substance abuse,17 although a separate analysis (some versus frequent use) did not find that substance use affected adherence.27 In a study among MSM using PrEP in Boston, barriers to PrEP uptake and adherence differed by type of substance used. Stimulant users were more likely to be concerned that substance use would affect adherence, and were less concerned about HIV stigma as a barrier to PrEP uptake, compared with alcohol users. Barriers to PrEP uptake and adherence differed by type of substance used.28

Higher sex-related PrEP adherence was associated with older age groups, and after adjustment by other correlates, college completion showed significantly higher sex-related PrEP adherence than less education. Older MSM have been found to have higher PrEP drug concentrations in previous trials,29 and we speculate that both of these findings could be related to a higher knowledge base concerning HIV-related issues and/or strategic decision-making capacity in the face of risk. In our study, adherence was lower in those with a higher frequency of sex events.

Surprisingly, independent of any association with stimulant substance use and number of sex events, moderate to heavy drinking (high AUDIT score at screening) was associated with higher sex-related PrEP adherence among the MSM in our study. Hazardous and harmful alcohol consumption using the AUDIT score has been found in 8% of the Thai population.30 Moderate to heavy alcohol use has been well-documented in MSM populations,31 and associated with riskier sexual behavior, such as increased odds of sex with a nonprimary partner,32 greater odds of having anal intercourse without a condom regardless of HIV status,33 and increased risk of HIV acquisition,34 In the general population of people with HIV, alcohol consumption shows a significant and consistent association with nonadherence to ART.16,35,36 Alcohol use disorders have been shown to negatively influence adherence among MSM in Peru.37 However, in some studies of HIV-infected adults, when compared with nonalcohol drug use, alcohol dependence was not associated with suboptimal medical adherence.38 In addition, among binge-drinking HIV-infected persons, adherence to ART was worse on weekends, but not appreciably worse compared with use on weekdays.39 In sum, it is possible that alcohol use may not be as large a barrier to PrEP adherence in an HIV prevention context as it is for ART in a treatment context. This topic is worthy of further investigation.

Variables that may have influenced greater sex-related PrEP adherence among moderate to heavy drinkers could have been the timing of drinking, and whether binge drinking was common among this small group. We know that social context moderates the effect of alcohol consumption on choice of partner type and the use of protection methods (barrier and possibly now pharmacologic).32 Heavy drinking with expected sexual activity, associated with specific venues, may have resulted in greater prevention agency, and thus higher sex-related PrEP adherence among our participants. Clearly, more needs to be understood about substance and alcohol use, and use of PrEP.

This study has several limitations. Although high adherence to PrEP has been observed in the context of ongoing clinical services and longitudinal studies, at the time this study occurred, the CDC recommendation to take PrEP was for daily dosing. Before the results of the Ipergay study's nondaily dosing regimen were released, the lack of evidence on nondaily dosing may have undermined motivation to use nondaily regimens. In addition, sex-related PrEP adherence by event-driven dosing may not have been supported by societal and cultural factors, and as our qualitative data suggest, it is a harder regimen to follow (personal communication from T. Chemnasiri). All adherence measures were limited by self-reported measurement of sex events and pill taking, and we assessed sex-related PrEP adherence without the use of plasma concentrations or dried blood spots. Self-reported data on PrEP adherence can be inaccurate when compared with drug levels, thus coverage data may be an overestimate. In addition, we understood that depending on the order that interviewers asked about adherence and sex, participants may have reported a fewer number of sex events to align with adherence. Therefore, interviews were conducted by those not engaged with provision of care, and were trained in neutral interviewing practice. We attempted to minimize biases introduced during participant interviews by using a standard neutral interview approach, as outlined in the methods.

We recognize that sex-related PrEP adherence is insufficient to approximate efficacy. Importantly, the study did not collect data on the timing of alcohol use, on use by venue type (social, congregate, isolated), or on sexual activity with substance use by venue type. In addition, substance users may have performed less well in reporting adherence. Finally, there were not enough TGW enrolled in the study to make any conclusions about correlates associated with their sex-related PrEP adherence.

Most countries with PrEP policies in place have recommended daily dosing, including the latest US CDC updated guidelines on PrEP.40 In a clinical setting, starting and stopping PrEP should be a decision made between HIV-negative people who are at substantial risk of HIV infection and their provider. In this trial, regardless of substance use, Thai MSM and TGW followed the regimen dosing schedules to provide good sex-related PrEP adherence that can inform future trials in this setting. Older age and higher educational level were significant correlates of higher sex-related PrEP adherence. These factors, if found to be important predictors of daily or nondaily PrEP use in nonresearch settings, change slowly and predictably. Conversely, relationship status, sexual frequency, and practices including use of condoms, and use of substances associated with sexual activity are behaviors that can change frequently and may be appropriate targets for short-term intervention. The correlates of lower adherence may affect PrEP use in persons choosing to use off-label dosing regimens, particularly event-driven dosing. Researchers of future PrEP trials should monitor substance use carefully, particularly use of alcohol and stimulants, and consider the impact these substances can have in future efficacy trials of nondaily PrEP.


The authors would like to thank all the study participants who participated in HPTN 067/ADAPT, and all the staff at the Silom Community Clinic who worked on this trial. The authors remember the lives and work of Supaporn Chaikummao and Patrick J. Flaherty, who devoted their professional lives to service and research among those who were most at risk of HIV infection.


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HIV; event-driven; PrEP; men who have sex with men; Thailand

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