After multiple clinical trials demonstrated its efficacy [1–4], preexposure prophylaxis (PrEP) with oral tenofovir (TFV) disoproxil fumarate/emtricitabine (TDF/FTC) is now broadly recommended by the Centers for Disease Control and Prevention  and the WHO  to prevent HIV acquisition. The measurement of PrEP drug levels in plasma (as an objective metric of adherence) proved critical to interpreting the effectiveness of PrEP in the clinical trials [1,7–9]. However, plasma measures of TFV and FTC represent short-term exposure and are susceptible to ‘white coat’ (short-term improvement in) adherence patterns . Concentrations of TFV and/or FTC (or their metabolites) in dried blood spots (DBS)  and hair samples  measure longer term adherence and exposure, are highly correlated , are associated with both efficacy  and toxicities of PrEP [15,16], and have therefore been increasingly incorporated as adherence metrics into PrEP programs during scale-up. As hair can be collected (even at home ) and stored at room temperature without biohazardous precautions, providing feasibility in the field, we sought to compare its utility as an alternative adherence measure to DBS in a large PrEP study.
The US PrEP demonstration project (PrEP Demo) enrolled a large cohort of MSM and transgender women in three US cities (Miami, San Francisco, Washington DC) for PrEP provision, collection of adherence measurements (including self-report and TFV–diphosphate concentrations in DBS), and testing for HIV and sexually transmitted infections . The incidence of HIV infection in this study was very low (0.43 per 100 person-years) and self-reported adherence high (87.4% across all visits). The DBS measures in PrEP Demo showed that participants took ≥4 doses a week (consistent with protective levels ) over ∼84% of visits. Factors associated with protective DBS levels in PrEP Demo were greater sexual risk (two condomless anal sex partners in the past 3 months) and stable housing, whereas being African-American or enrollment at the Miami site were associated with lower DBS levels .
As modest but statistically significant declines in renal function with administration of daily TDF/FTC have been observed in the PrEP clinical trials and demonstration projects [19–21], the association between drug exposure and decline in renal function is also of interest. In the Preexposure prophylaxis initiative (iPrEx) open label extension (OLE) study we showed a monotonic relationship between number of doses of TDF/FTC taken per week as estimated by hair levels and percentage decrease in creatinine clearance (CrCl) . In the full PrEP Demo cohort , the mean creatinine increased from baseline to week 12 by 0.03 mg/dl (4.6%; P < 0.0001) and the mean CrCl decreased by 4.76 ml/min (3.0%; P < 0.0001). These changes remained stable through week 48 and greater declines in renal function were associated with higher DBS concentrations of PrEP drugs .
A subset of participants in PrEP Demo opted into the ‘Enhancing PrEP in Community’ (EPIC) hair study, which collected quarterly hair samples for adherence monitoring. This analysis presents the results on the hair metrics in the EPIC hair study, examining in this large study concordance between DBS and hair levels, factors associated with higher concentrations of PrEP drugs in hair, and the relationship between drug exposure assessed by hair levels and renal function over time.
Study population and procedures
PrEP Demo enrolled 557 HIV-negative MSM and transgender women from sexually transmitted infection clinics in Miami and San Francisco and a community health center in Washington DC from October 2012 to January 2014 . Participants were provided TDF/FTC (300/200 mg)-based PrEP for free over 48 weeks and seen at weeks 4, 12, 24, 36, and 48. Demographics collected at baseline included age, race, sexual orientation and sex identification, educational level, knowledge of and attitudes toward PrEP, and income. Instruments assessing self-reported adherence, depression, drug and alcohol use, current housing status, and recent sexual behaviors were collected at each visit. Serum creatinine was measured quarterly and CrCl  was estimated by the Cockcroft–Gault equation . All Demo project participants were approached at their 12-week visit to participate in the EPIC hair study. For those who opted into and consented for this separate study, hair samples were collected every 12 weeks. For those who did not opt into the EPIC hair study, reasons for not participating were collected.
Using previously described methods, 100 strands of hair were cut from the occipital scalp  from EPIC participants with small scissors. Of note, the procedure for cutting the hair takes 2 min or less. After storage and shipment at ambient temperature from the different sites to our University of California San Francisco-based ‘Hair Analytical Laboratory’, the proximal 1.5 cm of each hair sample (representing ∼6-week exposure) was cut finely with scissors and 5 mg processed and analyzed using liquid chromatography/tandem mass spectrometry . The assays for measuring TFV and FTC in hair samples in the Hair Analytical Laboratory have been peer reviewed and approved by the Division of AIDS’ Clinical Pharmacology and Quality Assurance program .
Concordance of preexposure prophylaxis drug levels in hair and dried blood spots
The concordance of TFV–diphosphate in DBS and TFV in hair samples consistent with ≥4 doses/week of PrEP was tabulated after pooling study visits. The average number of tablets taken per week was estimated for each of the adherence measures and dichotomized into less than 4 doses/week and ≥4 doses/week. The number of doses taken per week based on participants’ hair concentrations used ‘adherence benchmarks’ established in a study called STRAND , where directly observed TDF was given to HIV-uninfected volunteers at 2, 4, and 7 doses a week (with wash-out periods in-between) and hair levels for those dosing patterns calculated . For DBS, dosing categories were based on a pharmacokinetic model  (recently confirmed with a directly observed dosing study)  of TFV–diphosphate concentrations. The concordance between hair and DBS PrEP drug concentrations around the threshold of four doses/week was calculated.
Definition of adequate adherence
In iPrEx OLE, there were no HIV seroconversions among participants with DBS TFV–diphosphate concentrations consistent with taking ≥4 doses/week (≥700 fmol/punch) . In EPIC, therefore, we defined adequate adherence as TFV levels in hair consistent with ≥4 doses/week (≥0.023 ng/mg as defined in STRAND ).
Factors associated with adequate preexposure prophylaxis adherence
We used mixed effects multivariate logistic regression models to examine factors associated with protective TFV hair levels across all visits. We first tested a number of covariates – both baseline (age, race/ethnicity, site of enrollment, sex, knowledge of and attitudes toward PrEP) and time varying (housing status, sexual behaviors, depression, drug and alcohol use) – in relationship to adequate adherence in univariate models. Any covariate that achieved a P value less than 0.10 in the univariate model was included in the final multivariate model.
Association between hair levels and declines in renal function
The percentage change in creatinine or CrCl from the baseline value was estimated across all visits (mean ± 95% confidence interval) for each of four estimated doses/week categories by hair levels [<2 doses/week (<0.0096 ng/mg), 2–3 doses/week (0.0096 to< 0.0206 ng/mg), 4–6 doses/week (0.0206 to < 0.0370 ng/mg), daily dosing (≥0.0370 ng/mg)] from separate mixed effects models with no covariates (intercept only) and random person effects. To obtain a P value for trend across the categories of estimated doses per week, we assigned them integer scores of 1–4 and fit a model using all persons together with that score as the only predictor.
The study protocols for both PrEP demo and the EPIC hair study were approved by Institutional Review Boards at all participating sites and participants provided written informed consent. Results of hair testing were not reported back to EPIC participants. Gilead Sciences (Foster City, California, USA) donated study drug and had no input into the study.
Demographics of enhancing preexposure prophylaxis in community participants
Of the 507 participants in PrEP Demo approached to participate in the EPIC hair study, 294 (58%) enrolled, with 280 (55%) of those staying in the study and providing hair. The main reasons for not wanting to join the EPIC hair study (n = 213) were related to concerns regarding hair collection (27% worried about hair style disruption; 61% concerned about not having enough hair; 2% worried collection could hurt) or not having enough time (9%). Only 1% of participants were concerned about hair levels revealing poor adherence to the study investigators.
Table 1 summarizes the baseline characteristics of the EPIC hair study participants (n = 280). Demo participants who did not enroll in the EPIC hair study were significantly more likely to be from the Miami site (P < 0.001) and have lower educational levels (P 0.026), were less likely to report condomless receptive anal sex (P 0.0012) or use recreational drugs (P 0.0013), and were less likely to be adherent to PrEP by both self-report (P 0.0007) and by DBS drug level data (P < 0.001). Among the enrollees who entered EPIC, hair data was available for a total of 875 person-visits for these 280 participants (mean three samples/participant). The median age of participants was 34 (range 19–65) years; 99% were MSM; 71% reported condomless receptive anal sex in the past 3 months; and 60% reported recreational drug use (13% amphetamine) in the last 3 months. Among 875 person-visits with hair data, hair levels were ≥0.023 ng/mg, consistent with ≥4 doses/week [14,15], 87% of the time.
Concordance of ≥4 preexposure prophylaxis doses/week in hair and dried blood spots
We had DBS and hair concentrations at the same visits in 444 person-visits. The concordance of levels of TFV in hair and TFV–diphosphate in DBS consistent with taking ≥4 PrEP doses/week in these visits was 84.3% (76.6% both ≥4 doses/week; 7.7% both less than four doses/week; 10.8% less than four doses/week in hair but ≥4 doses/week in DBS; 4.9% ≥4 doses/week in hair but <4 doses/week in DBS).
Factors associated with adequate adherence
Several factors were examined in univariate analyses in relationship to hair TFV levels consistent with taking ≥4 doses/week. Table 2 shows the factors associated with adequate adherence in both univariate and multivariate analyses. In univariate analyses, increasing age, use of amphetamines in the last 3 months, not being from the Miami site, having a stable living situation over the past 3 months, and reporting condomless receptive anal sex over the past 3 months were all associated with adequate adherence (all P < 0.10). Being African-American was not associated with adherence in univariate analyses and not included in the final models. In the multivariate model, not being from the Miami site (P 0.22) and increasing age (per decade, P 0.14) no longer stayed significantly associated with hair levels consistent with ≥4 doses/week. Using amphetamines over the past 3 months maintained a trend toward a higher odds of adequate adherence (P 0.06). Condomless receptive anal sex over the past 3 months maintained a significant association with adherence (P 0.01). And finally, more unstable housing (living in a friend or family member's abode instead of a house or apartment one rents or owns) maintained its association with a lower odds of achieving adequate adherence in multivariate models (P 0.04).
Relationship between hair concentrations of tenofovir and changes in creatinine clearance
Another study within PrEP Demo examines the factors associated with changes in CrCl over time , so our analysis was restricted to examining the relationship between dosing patterns as assessed by hair levels among EPIC hair study participants and mean percentage changes in creatinine or CrCl across all visits.
Among the 875 person-visits with hair data, 859 had concomitant creatinine measurements. Approximately 4.4% (38/859) of these person-visits had hair levels consistent with less than 2 pills/week; 8.6% (n = 74) had levels consistent with 2–3 pills/week; 44% (n = 378) had levels consistent with 4–6 pills/week; and 43% (n = 369) had levels consistent with daily dosing. There was a monotonic relationship between increasing use of PrEP and both mean percentage decrease in CrCl from baseline (Fig. 1a) and mean percentage increase in creatinine from baseline (Fig. 1b) across all visits (P 0.011 and 0.030 for trends, respectively). For participants in the EPIC hair study, the percentage of visits where CrCl fell to 60 or 70 ml/min or less was low (0 and 0.3%, respectively).
This is one of the largest studies to examine hair levels of TFV/FTC as an adherence measure among MSM on PrEP. Long-term adherence metrics in the setting of PrEP use have the potential to identify those in need of adherence intervention to increase the effectiveness of PrEP. Hair collection has some feasibility advantages in the field as no phlebotomy or cold chain is required and hair samples can be self-collected . In this substudy of the U.S. Demo project, we demonstrated that DBS and hair concentrations of PrEP drugs were highly concordant (84%) and that high-risk behavior (condomless receptive anal sex and amphetamine use), and a more stable living situation were associated with higher levels of adherence to PrEP drugs as adjudicated by hair levels. Furthermore, we found a greater decline in renal function (and greater increases in creatinine) from baseline with higher hair levels of PrEP drugs.
Our findings of relatively high adherence levels in the EPIC hair study by hair concentrations (87% of person-visits had hair levels consistent with ≥4 doses/week) were very similar to the adherence assessment provided by DBS measures in the overall PrEP Demo cohort (84% of person-visits with DBS levels consistent with ≥4 doses/week) . Although objective adherence measures showed low adherence to study product in the placebo-controlled trials of TDF/FTC, when the effectiveness of PrEP to prevent HIV acquisition was unknown, adherence to PrEP in open-label studies and demonstration projects, after PrEP was proven effective and approved by a variety of regulatory bodies around the world [5,6], has been high [14,18,27,28], especially among MSM at high risk. PrEP Demo reported similar factors associated with higher levels of adherence as measured by DBS concentrations as we report in the EPIC hair study, namely higher risk behaviors (e.g., condomless anal sex), stable housing, and older age (trend in both studies) .
Long-term pharmacologic measures not only assess behavior (e.g., adherence or drug taking), but also serve as direct measures of pharmacokinetic exposure, which can be useful when monitoring for the known toxicities of TDF/FTC-based therapy, specifically renal toxicity  and declines in bone mineral density . In iPrEx OLE, hair concentrations of TFV predicted renal decline ; in the randomized iPrEx trial, higher concentrations of intracellular TFV–diphosphate in peripheral blood mononuclear cells were associated with greater declines in CrCl  or bone mineral density ; and in the PrEP Demo project both DBS concentrations of TFV–diphosphate and hair levels of TFV and FTC were associated with declines in CrCl and increases in creatinine over time . These associations between PrEP drug exposure and renal decline stress the need for vigilant attention to monitoring CrCl regularly to ensure safety; indeed, patients with high levels of adherence to daily dosing may require more frequent monitoring .
Studies are often choosing either hair monitoring, DBS monitoring, or both to examine patterns of adherence to PrEP drugs as PrEP rolls out across the globe. The choice of one measure over another is often made based on feasibility in the field. Like hair, DBS are easy to collect, but require phlebotomy, a cold chain, and biohazardous precautions. DBS concentrations of TFV–diphosphate and FTC–triphosphate can provide information on both longer term and shorter term patterns of adherence , as can the segmental analyses of hair samples . Hair collection has varying levels of acceptability to participants for sampling, however, depending on study design. In this ‘opt-in’ study, acceptability was only 58%. Of note, many participants who declined to participate were from the Miami site where hair is often worn very short (although collection from even very short hair yields testable samples). Although 9% participants perceived hair collection would take too much time, the procedure takes less than 2 min, which can be counseled to field staff and participants to mitigate this widely held misperception.
By contrast, in a study of young MSM where hair collection was ‘opt-out’ (Adolescent Trials Network studies 110 and 113), the hair collection rate was more than 95% . In other studies where hair collection is incorporated early in the protocol and the field staff trained that hair can be collected from very short hair, takes very little time, and does not disrupt hair styles, acceptability has been very high [31–33]. New data that self-collected hair yields similar concentration data to hair collected in the field  may enhance the acceptability of this measure. Of importance in this study was that only 1% of participants were concerned about providing a sample that could reveal their adherence level. Moreover, other studies have suggested that provision of drug levels could improve subsequent drug taking [34,35]. However, both DBS and hair require expensive liquid chromatography/ tandem mass spectrometry equipment for analyses and are performed in high-level research laboratories in the US. Lower cost methods that can be applied to real world implementation in the field and to assess drug taking using point-of-care technology will be the next advances in the field.
In sum, we demonstrate the utility of hair measures for adherence monitoring within a PrEP demonstration project among MSM and transgender women in the US, finding hair and DBS PrEP drug levels to be concordant, and confirming findings from the larger cohort that high-risk behavior likely encourages adherence to PrEP. As in the parent study and other studies , higher levels of PrEP use are associated with greater declines in renal function. As current US PrEP guidelines are not yet recommending anything less than daily dosing to achieve maximal PrEP efficacy, older patients with higher adherence patterns may require more frequent monitoring of CrCl to maximize safety in this population. Both DBS and hair measures can provide objective assessment of adherence and indicate high exposure levels associated with risk of toxicities, providing studies with choices on adherence metrics based on their setting, participant preference, and design. The provision of PrEP to at-risk individuals worldwide is integral to ending the HIV epidemic, and approaches to maximize efficacy and minimize adverse effects will aid in effective roll out.
The Demo Project was supported by grant UM1AI069496 from the National Institute for Allergies and Infectious Diseases (NIAID). The Enhancing PrEP in Community (EPIC) study was supported by NIMH/NIH (R01 MH095628, P.I. Albert Liu). The hair assays for this study were supported by NIAID/NIH (2R01 AI098472, P.I. Monica Gandhi). Statistical support was partially provided by UCSF CTSI grant#UL1 TR000004. This work was also supported the Eunice Kennedy Shriver National Institute of Child Health and Human Development [K12 HD052163 (P.I. C. Brindis, N. Adler) to support C.A.K.] and the National Institute of Mental Health (T32 MH19105–28 to support P.M.M.). We thank the participants of the Demo Project and the dedicated study staff. We also thank Nhi Phung, Dr Hideaki Okochi, and Josh Lacanienta from the UCSF HAL. We acknowledge and are grateful to Hao Zhang, MD (program officer at NIAID for 2R01 AI098472) for his invaluable support and scientific input; Meeting at which this work was presented: Conference on Retroviruses and Opportunistic Infections, 13–16 February 2017; Seattle, Washington, USA; Abstract 978; Gilead Science (Foster City, California, USA) donated FTC/TDF for participants in the study and paid for the DBS assays, but provided no other financial support and did not contribute to data interpretation or manuscript development.
Conflicts of interest
There are no conflicts of interest.
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