Publications by authors named "Samantha E Dilworth"

60 Publications

An autoregressive cross-lagged model unraveling co-occurring stimulant use and HIV: Results from a randomized controlled trial.

Drug Alcohol Depend 2021 Aug 3;225:108752. Epub 2021 Jun 3.

Department of Public Health Sciences, University of Miami Miller School of Medicine, Miami, FL, USA. Electronic address:

Background: Evidence-based interventions are needed to address the use of stimulants such as methamphetamine as a driver of onward HIV transmission and faster clinical HIV progression among sexual minority men. Prior randomized controlled trials with people living with HIV who use substances indicate that financial incentives provided during contingency management (CM) are effective for achieving short-term reductions in stimulant use and HIV viral load. However, the benefits of CM are often not maintained after financial incentives for behavior change end.

Purpose: Data from a recently completed randomized controlled trial with 110 sexual minority men living with HIV who use methamphetamine was leveraged to examine mediators of the efficacy of a positive affect intervention for extending the benefits of CM.

Methods: An autoregressive cross-lagged model was fit to determine if reductions in HIV viral load were mediated by intervention-related increases in positive affect and decreases in stimulant use measured in four waves over 15 months.

Results: Higher baseline positive affect predicted significantly lower self-reported stimulant use immediately following the 3-month CM intervention period, even after controlling for self-reported stimulant use at baseline. Moreover, decreased stimulant use emerged as an independent predictor of long-term reductions HIV viral load at 15 months, even after adjusting for HIV viral load at baseline and the residual effect of the positive affect intervention.

Conclusions: Findings underscore the importance of durable reductions in stimulant use as a primary intervention target that is essential for optimizing the clinical and public health benefits of HIV treatment as prevention.
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http://dx.doi.org/10.1016/j.drugalcdep.2021.108752DOI Listing
August 2021

A mindfulness-based, stress and coping model of craving in methamphetamine users.

PLoS One 2021 18;16(5):e0249489. Epub 2021 May 18.

School of Medicine, University of Miami, Coral Gables, Florida, United States of America.

There is increasing interest in the role of mindfulness and mindfulness-based interventions to optimize recovery from a substance use disorder (SUD). However, relatively little is known about the theory-based psychological and social pathways whereby mindfulness could have beneficial effects for managing a chronic, relapsing SUD. Informed by Revised Stress and Coping Theory, the present cross-sectional study examined affective, cognitive, and social pathways whereby mindfulness is associated with lower methamphetamine craving. A total of 161 HIV-positive, methamphetamine-using sexual minority men completed a screening visit for a randomized controlled trial. Using a hybrid structural equation model, we examined pathways whereby mindfulness is associated with lower methamphetamine craving. We found that greater mindfulness was directly associated with lower negative affect and higher positive affect as well as indirectly associated with less methamphetamine craving. Interestingly, the indirect association between mindfulness and methamphetamine craving appeared to be uniquely attributable to positive affect. Only positive affect was indirectly associated with lower methamphetamine craving via higher positive re-appraisal coping and greater self-efficacy for managing triggers for methamphetamine use. Methamphetamine craving was supported by moderate associations with greater substance use severity and more frequent methamphetamine use. These findings support the role of mindfulness in cultivating positive affect, which could be crucial to build the capacity of individuals to manage methamphetamine craving as a chronic stressor that threatens recovery from SUD.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0249489PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8130914PMC
May 2021

Internalized HIV Stigma Predicts Suboptimal Retention in Care Among People Living with HIV in the United States.

AIDS Patient Care STDS 2021 05 22;35(5):188-193. Epub 2021 Apr 22.

Division of HIV, ID, and Global Medicine, University of California San Francisco, San Francisco, California, USA.

HIV-related stigma is a known barrier to retention in care. However, no large-scale, multi-site studies have prospectively evaluated the effect of internalized stigma on retention in care. The Centers for AIDS Research Network of Integrated Clinical Systems (CNICS) cohort study integrates medical record and survey data from people living with HIV (PLWH) seen in HIV primary care clinics across the United States, and assesses internalized stigma yearly using a validated 4-item Likert scale. We used multivariable logistic regression models to evaluate associations between mean internalized stigma and two prospective retention in care outcomes: keeping the next primary care appointment and keeping all scheduled primary care appointments in the 12 months following stigma assessment. From February 2016 to November 2017, 5968 PLWH completed the stigma assessment and had adequate follow-up time. Mean stigma was 1.9 (standard deviation 1.08). Increased mean stigma scores were associated with decreased odds of attending the next primary care appointment [adjusted odds ratio (aOR) = 0.93, 95% confidence interval (CI) 0.88-0.99,  = 0.02], and all primary care appointments in the subsequent 12 months (aOR = 0.94, 95% CI 0.89-0.99,  = 0.02). In both models, younger age and Black race were also independently associated with suboptimal appointment attendance. There was no support for interactions between internalized stigma and covariates. Internalized HIV stigma had an independent negative effect on the odds of subsequent appointment attendance. This study highlights the importance of identifying even low levels of internalized stigma. Interventions to address internalized HIV stigma are critical to supporting retention in care and improving clinical outcomes.
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http://dx.doi.org/10.1089/apc.2020.0244DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8106244PMC
May 2021

Intersecting minority statuses and tryptophan degradation among stimulant-using, sexual minority men living with HIV.

J Consult Clin Psychol 2021 Mar;89(3):156-165

Department of Community Health Systems.

Background: Disclosure of one's sexual orientation as a sexual-minority (SM) person (i.e., being "out") may affect HIV-related health outcomes. This longitudinal study examined whether race/ethnicity moderated effects of outness on the plasma kynurenine/tryptophan (KT) ratio, a marker of dysregulated serotonin metabolism due to immune activation that predicts clinical HIV progression.

Methods: Participants were African American, Hispanic/Latino, and non-Hispanic White, methamphetamine-using SM men living with HIV (N = 97) who completed self-report scales of outness and SM stress at baseline for a randomized controlled trial of a positive affect intervention. Linear mixed modeling was used to test whether race/ethnicity and experimental condition moderated the association of baseline outness with the KT ratio at baseline, 6, 12, and 15 months controlling for SM stress, sociodemographics, HIV disease markers, and recent stimulant use.

Results: The interactions of outness by race/ethnicity and outness by experimental condition on the KT ratio were significant. Greater outness predicted a lower KT ratio over time in non-Hispanic White SM men, but not among SM men of color (MOC). Greater outness predicted a lower KT ratio over time for SM men in the control, but not among those in the intervention arm.

Conclusion: Being more out may be protective for non-Hispanic White SM men, but not for their SM MOC peers. Outness mattered for participants who did not receive the positive affect intervention. Findings underscore the potentially different contexts and consequences of outness depending on SM men's race/ethnicity and whether they received a positive affect intervention. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
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http://dx.doi.org/10.1037/ccp0000586DOI Listing
March 2021

Measuring Satisfaction and Comfort with Gender Identity and Gender Expression among Transgender Women: Development and Validation of the Psychological Gender Affirmation Scale.

Int J Environ Res Public Health 2021 03 23;18(6). Epub 2021 Mar 23.

Center for AIDS Prevention Studies, Department of Medicine, University of California, San Francisco, CA 94158, USA.

Among transgender and gender diverse people, psychological gender affirmation is an internal sense of valuing oneself as a transgender or gender diverse person, being comfortable with one's gender identity, and feeling satisfied with one's body and gender expression. Gender affirmation can reduce gender dysphoria and mitigate deleterious health effects of marginalization. We sought to create an instrument to measure psychological gender affirmation among transgender women. Following initial item development using qualitative interviews, we used self-administered survey data from two distinct samples ( = 278; = 368) of transgender women living with HIV in the USA. We used data from Study 1 to perform exploratory factor analysis (EFA) and data from Study 2 to perform confirmatory factor analysis (CFA), yielding the five-item single-factor Psychological Gender Affirmation (PGA) scale with high reliability (α = 0.88). This scale is psychometrically sound as demonstrated by its convergent and discriminant validity via correlations with select measures and by its predictive validity through associations in hypothesized directions with measures of mental health and substance use. The PGA scale will aid research on psychological gender affirmation that can in turn inform interventions as well as gender-affirming clinical and social practices to promote the health and well-being of transgender and gender diverse people.
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http://dx.doi.org/10.3390/ijerph18063298DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8005192PMC
March 2021

Measuring Satisfaction and Comfort with Gender Identity and Gender Expression among Transgender Women: Development and Validation of the Psychological Gender Affirmation Scale.

Int J Environ Res Public Health 2021 03 23;18(6). Epub 2021 Mar 23.

Center for AIDS Prevention Studies, Department of Medicine, University of California, San Francisco, CA 94158, USA.

Among transgender and gender diverse people, psychological gender affirmation is an internal sense of valuing oneself as a transgender or gender diverse person, being comfortable with one's gender identity, and feeling satisfied with one's body and gender expression. Gender affirmation can reduce gender dysphoria and mitigate deleterious health effects of marginalization. We sought to create an instrument to measure psychological gender affirmation among transgender women. Following initial item development using qualitative interviews, we used self-administered survey data from two distinct samples ( = 278; = 368) of transgender women living with HIV in the USA. We used data from Study 1 to perform exploratory factor analysis (EFA) and data from Study 2 to perform confirmatory factor analysis (CFA), yielding the five-item single-factor Psychological Gender Affirmation (PGA) scale with high reliability (α = 0.88). This scale is psychometrically sound as demonstrated by its convergent and discriminant validity via correlations with select measures and by its predictive validity through associations in hypothesized directions with measures of mental health and substance use. The PGA scale will aid research on psychological gender affirmation that can in turn inform interventions as well as gender-affirming clinical and social practices to promote the health and well-being of transgender and gender diverse people.
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http://dx.doi.org/10.3390/ijerph18063298DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8005192PMC
March 2021

Cocaine Use and White Matter Hyperintensities in Homeless and Unstably Housed Women.

J Stroke Cerebrovasc Dis 2021 May 5;30(5):105675. Epub 2021 Mar 5.

University of California, San Francisco, Department of Radiology and Biomedical Imaging, San Francisco, CA, USA. Electronic address:

Objectives: Cocaine use has been linked to stroke in several studies. However, few studies have considered the influence of cocaine use on stroke mechanisms such as small vessel disease (SVD). We conducted a study to assess associations between the toxicology-confirmed use of multiple drugs, including cocaine, and a marker of SVD, white matter hyperintensities (WMH).

Materials And Methods: We conducted a nested case-control study (n = 30) within a larger cohort study (N = 245) of homeless and unstably housed women recruited from San Francisco community venues. Participants completed six monthly study visits consisting of an interview, blood draw, vital sign assessment and baseline brain MRI. We examined associations between toxicology-confirmed use of multiple substances, including cocaine, methamphetamine, heroin, alcohol and tobacco, and WMH identified on MRI.

Results: Mean study participant age was 53 years, 70% of participants were ethnic minority women and 86% had a history of cocaine use. Brain MRIs indicated the presence of WMH (i.e., Fazekas score>0) in 54% (18/30) of imaged participants. The odds of WMH were significantly higher in women who were toxicology-positive for cocaine (Odd Ratio=7.58, p=0.01), but not in women who were toxicology-positive for other drugs or had several other cerebrovascular risk factors.

Conclusions: Over half of homeless and unstably housed women showed evidence of WMH. Cocaine use is highly prevalent and a significant correlate of WMH in this population, while several traditional CVD risk factors are not. Including cocaine use in cerebrovascular risk calculators may improve stroke risk prediction in high-risk populations and warrants further investigation.
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http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2021.105675DOI Listing
May 2021

Tryptophan depletion predicts lower positive affect in sexual minority men living with HIV who use methamphetamine.

J Neurovirol 2021 02 18;27(1):178-182. Epub 2021 Jan 18.

Department of Public Health Sciences, University of Miami Miller School of Medicine, Miami, FL, 33136, USA.

This longitudinal study with 76 sexual minority men living with HIV who use methamphetamine examined whether dysregulation of essential amino acid precursors for neurotransmitters at baseline predicted positive and negative affect at 15 months. After controlling for covariates including baseline positive affect, a higher baseline kynurenine/tryptophan (K/T) ratio independently predicted lower positive affect at 15 months (β = - 18.31; 95% CI = - 35.35, - 1.27; p = 0.036). Future clinical research should examine whether bio-behavioral interventions targeting tryptophan degradation could optimize treatments for people living with co-occurring HIV and stimulant use disorders.
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http://dx.doi.org/10.1007/s13365-020-00937-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8071582PMC
February 2021

The HIV Index: Using a Patient-Reported Outcome on Engagement in HIV Care to Explain Sub-Optimal Retention in Care and Virologic Control.

Clin Infect Dis 2020 Dec 29. Epub 2020 Dec 29.

Department of Medicine, University of California, San Francisco, San Francisco, CA.

Background: We investigated the prospective association between a brief self-report measure of engagement in HIV care (the Index) and suboptimal retention and viral suppression (VS) outcomes.

Methods: The CNICS cohort study combines medical record data with patient-reported outcomes from eight HIV clinics in the United States, which from April 2016-March 2017 included the 10-item Index. Multivariable logistic regression (LR) was used to estimate the risk and odds ratios of mean Index score on two outcomes in the subsequent year: 1) not keeping at least 75% of scheduled HIV care appointments, and; 2) for those with VS at Index, having viral load >200 copies/mL on at least one measurement. We also employed generalized linear mixed models (GLMM) to estimate the risk and odds ratios of appointment non-attendance or unsuppressed viral load at any given observation. We generated receiver-operator characteristic (ROC) curves for the full models overlaid with Index as a sole predictor.

Results: Mean Index score was 4.5 (SD 0.6). Higher Index scores were associated with lower relative risk of suboptimal retention (N=2,576; LR aRR 0.88, 95% CI 0.87 - 0.88; GLMM aRR 0.85, 95% CI 0.83 - 0.87 and lack of sustained VS (N=2,499; LR aRR 0.75, 95% CI 0.68 - 0.83; GLMM aRR 0.74, 95% CI 0.68 - 0.80. Areas under the ROC curve for the full models were 0.69 (95% CI = 0.67 - 0.71) for suboptimal retention and 0.76 (95% CI = 0.72 - 0.79) for lack of sustained VS.

Conclusions: Index scores are significantly associated with suboptimal retention and VS outcomes.
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http://dx.doi.org/10.1093/cid/ciaa1892DOI Listing
December 2020

Gender Affirmation through Correct Pronoun Usage: Development and Validation of the Transgender Women's Importance of Pronouns (TW-IP) Scale.

Int J Environ Res Public Health 2020 12 19;17(24). Epub 2020 Dec 19.

Center for AIDS Prevention Studies, Department of Medicine, University of California, San Francisco, CA 94158, USA.

Social interactions where a person is addressed by their correct name and pronouns, consistent with their gender identity, are widely recognized as a basic and yet critical aspect of gender affirmation for transgender people. Informed by the Model of Gender Affirmation, we developed a self-report measure of the importance of social gender affirmation, the Transgender Women's Importance of Pronouns (TW-IP) scale, which measures gender affirmation through the usage of correct pronoun by others. Data were from self-administered surveys in two independent samples of transgender women living with HIV in the US (N1 = 278; N2 = 369). Using exploratory factor analysis with data from Study 1 and confirmatory factor analysis with data from Study 2, we obtained a four-item scale with a single-factor structure and strong reliability (α = 0.95). We present evidence of TW-IP's convergent and discriminant validity through its correlations with select mental health and HIV-related measures. Further, scores on TW-IP were linked in expected directions to several hypothesized mental health and HIV care outcomes, demonstrating its predictive validity. The resulting brief measure of importance of pronouns among transgender women shows strong psychometric properties. Validation evidence offers highly promising opportunities for use of the measure in clinical and research settings.
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http://dx.doi.org/10.3390/ijerph17249525DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7766835PMC
December 2020

Blue Monday: Co-occurring Stimulant Use and HIV Persistence Predict Dysregulated Catecholamine Synthesis.

J Acquir Immune Defic Syndr 2021 Mar;86(3):353-360

Department of Public Health Sciences, Miller School of Medicine, University of Miami, Miami, FL.

Background: This longitudinal study examined whether co-occurring stimulant use and HIV disease processes predicted greater risk for depression via dysregulated metabolism of amino acid precursors for neurotransmitters.

Methods: In total, 110 sexual minority men (ie, gay, bisexual, and other men who have sex with men) living with HIV who had biologically confirmed recent methamphetamine use were enrolled in a randomized controlled trial. The kynurenine/tryptophan (K/T) and phenylalanine/tyrosine (P/T) ratios were measured over 15 months to index dysregulated metabolism of amino acid precursors for serotonin and catecholamines. Markers of gut-immune dysregulation such as lipopolysaccharide binding protein and soluble CD14 (sCD14), HIV persistence in immune cells (ie, proviral HIV DNA), and stimulant use were examined as predictors. These bio-behavioral measures, including the K/T and P/T ratios, were also examined as predictors of greater risk for depression over 15 months.

Results: Higher time-varying sCD14 levels (β = 0.13; P = 0.04) and time-varying detectable viral loads (β = 0.71; P < 0.001) were independent predictors of a higher K/T ratio. Time-varying reactive urine toxicology results for stimulants (β = 0.53; P < 0.001) and greater proviral HIV DNA at baseline (β = 0.34; P < 0.001) independently predicted an increased P/T ratio. Greater time-varying, self-reported methamphetamine use uniquely predicted higher odds of screening positive for depression (Adjusted Odds Ratio = 1.08; 95% confidence interval: 1.01 to 1.17).

Conclusions: Ongoing stimulant use and HIV persistence independently predict dysregulated metabolism of amino acid precursors for catecholamines, but this did not explain amplified risk for depression.
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http://dx.doi.org/10.1097/QAI.0000000000002560DOI Listing
March 2021

Tryptophan degradation is associated with risk-taking propensity in methamphetamine users with treated HIV infection.

J Neurovirol 2020 10 29;26(5):779-784. Epub 2020 Jul 29.

Public Health Sciences and Psychology, Department of Public Health Sciences, University of Miami Miller School of Medicine, 1120NW 14th St. Office 1005, Miami, FL, 33136, USA.

Few studies have examined neuroimmune pathways that could contribute to impulsivity in people living with HIV who use substances. Eighty-four methamphetamine-using, sexual minority men with an undetectable HIV viral load were administered the Balloon Analogue Risk Task (BART), a behavioral measure of risk-taking propensity. We examined the associations between kynurenine/tryptophan ratio and phenylalanine/tyrosine ratio with BART scores using multiple linear regression. A higher kynurenine/tryptophan ratio was independently associated with greater BART scores (beta = 0.25; 95% CI = 0.05-1.23; p = 0.034). The phenylalanine/tyrosine ratio was not significantly associated with BART scores. Findings support the need for further research to elucidate the neuroimmune mechanisms linking tryptophan degradation with impulsivity to catalyze the development novel pharmacologic treatments for people living with HIV who use methamphetamine.
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http://dx.doi.org/10.1007/s13365-020-00841-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7541781PMC
October 2020

Getting to the point: Methamphetamine injection is associated with biomarkers relevant to HIV pathogenesis.

Drug Alcohol Depend 2020 Jun 18;213:108133. Epub 2020 Jun 18.

University of Miami School of Medicine, United States. Electronic address:

Background: People living with HIV who use stimulants, such as methamphetamine, display greater immune dysregulation and experience faster clinical HIV progression. However, it remains unclear if the extent of immune dysregulation differs between methamphetamine users who engage in injection drug use (Meth IDU) and methamphetamine users who do not.

Methods: This cross-sectional study enrolled 86 sexual minority men living with HIV who had an undetectable viral load (< 40 copies/mL) and recent, biologically confirmed methamphetamine use. Meth IDU participants were compared to methamphetamine users who did not report IDU with respect to microbial translocation, immune activation, and inflammation plasma biomarkers. Multiple linear regression models were adjusted for age, antiretroviral therapy regimen, CD4 + T-cell count, and reactive urine toxicology results (Tox+) for stimulants.

Results: The Meth IDU participants were significantly more likely to be homeless and Tox + for stimulants. In adjusted analyses, those reporting Meth IDU displayed elevated plasma levels of lipopolysaccharide binding protein (LBP), soluble CD163 (sCD163), interleukin-6 (IL-6), and soluble tumor necrosis factor - alpha receptor I (sTNF-αRI).

Discussion: Even among methamphetamine users with treated HIV, those who engage in Meth IDU display exacerbations in key pathophysiologic processes that are linked to faster clinical HIV progression. These findings highlight the importance of screening for Meth IDU, discussing safer injection practices, and providing linkages to needle exchanges to reduce the harms of Meth IDU. Those who are not ready, willing, or able to abstain from methamphetamine use could also derive important health benefits from avoiding Meth IDU.
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http://dx.doi.org/10.1016/j.drugalcdep.2020.108133DOI Listing
June 2020

Measuring engagement in HIV care: Measurement invariance in three racial/ethnic patient groups.

Health Psychol 2020 Jul 13;39(7):622-631. Epub 2020 Apr 13.

Center for AIDS Prevention Studies, Division of Prevention Science, Department of Medicine, University of California, San Francisco.

The objective of the study was to evaluate a novel measure of HIV care engagement in a large sample of non-Latino White, Latino, and African American patients. The Index of Engagement in HIV care (the Index) measures the degree to which a patient feels engaged/disengaged from HIV care. However, its measurement invariance, or the degree to which observed scores can be meaningfully compared across racial/ethnic groups, has not been established. The 10-item Index is a self-report measure initially validated in the Center for AIDS Research Network of Integrated Systems cohort study. Using Center for AIDS Research Network of Integrated Systems survey data, Index scores were linked to patients' electronic medical records, which included viral load (VL) and appointment attendance data. We conducted measurement invariance analyses to test the Index's performance in the 3 racial/ethnic groups and its cross-sectional association with VL and retention in HIV care (2 primary outcomes). A total of 3,127 patients completed the Index, which showed good reliability across the 3 groups (alphas >.84). Confirmatory factor analysis model fit statistics showed that the Index demonstrated configural, metric, and scalar invariance, supporting the conclusion that the Index is a single factor construct. Lastly, lower Index scores associated with a concurrent detectable VL and poor retention in HIV care for all 3 groups. Having demonstrated invariance, the Index scores can be used to compare engagement levels across non-Latino Whites, Latinos, and African Americans in HIV care settings. Improving HIV care retention requires tools that can accurately identify people struggling to stay engaged in HIV care, especially racial/ethnic minorities. (PsycInfo Database Record (c) 2020 APA, all rights reserved).
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http://dx.doi.org/10.1037/hea0000865DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7386898PMC
July 2020

Violence and Emergency Department Use among Community-Recruited Women Who Experience Homelessness and Housing Instability.

J Urban Health 2020 02;97(1):78-87

Department of Psychiatry, University of California, San Francisco, San Francisco, CA, USA.

Women who experience housing instability are at high risk for violence and have disproportionately high rates of emergency department (ED) use. However, little has been done to characterize the violence they experience, or to understand how it may be related to ED use. We recruited homeless and unstably housed women from San Francisco shelters, free meal programs, and single room occupancy (SRO) hotels. We used generalized estimating equations to examine associations between violence and any ED use (i.e., an ED visit for any stated reason) every 6 months for 3 years. Among 300 participants, 44% were African-American, and the mean age was 48 years. The prevalence of violence experienced in the prior 6 months included psychological violence (87%), physical violence without a weapon (48%), physical violence with a weapon (18%), and sexual violence (18%). While most participants (85%) who experienced physical violence with a weapon or sexual violence in the prior 6 months had not visited an ED, these were the only two violence types significantly associated with ED use when all violence types were included in the same model (OR = 1.83, 95% CI 1.02-3.28; OR = 2.15, 95% CI 1.30-3.53). Only violence perpetrated by someone who was not a primary intimate partner was significantly associated with ED use when violence was categorized by perpetrator. The need to reduce violence in this population is urgent. In the context of health care delivery, policies to facilitate trauma-informed ED care and strategies that increase access to non-ED care, such as street-based medicine, could have substantial impact on the health of women who experience homelessness and housing instability.
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http://dx.doi.org/10.1007/s11524-019-00404-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7010900PMC
February 2020

Randomized controlled trial of a positive affect intervention to reduce HIV viral load among sexual minority men who use methamphetamine.

J Int AIDS Soc 2019 12;22(12):e25436

Department of Medical Social Sciences, Northwestern University, Chicago, CA, USA.

Introduction: In the era of HIV treatment as prevention (TasP), evidence-based interventions that optimize viral suppression among people who use stimulants such as methamphetamine are needed to improve health outcomes and reduce onward transmission risk. We tested the efficacy of positive affect intervention delivered during community-based contingency management (CM) for reducing viral load in sexual minority men living with HIV who use methamphetamine.

Methods: Conducted in San Francisco, this Phase II randomized controlled trial tested the efficacy of a positive affect intervention for boosting and extending the effectiveness of community-based CM for stimulant abstinence to achieve more durable reductions in HIV viral load. From 2013 to 2017, 110 sexual minority men living with HIV who had biologically confirmed, recent methamphetamine use were randomized to receive a positive affect intervention (n = 55) or attention-control condition (n = 55). All individual positive affect intervention and attention-control sessions were delivered during three months of community-based CM where participants received financial incentives for stimulant abstinence. The 5-session positive affect intervention was designed to provide skills for managing stimulant withdrawal symptoms as well as sensitize individuals to natural sources of reward. The attention-control condition consisted of neutral writing exercises and self-report measures.

Results: Men randomized to the positive affect intervention displayed significantly lower log HIV viral load at six, twelve and fifteen months compared to those in the attention-control condition. Men in the positive affect intervention also had significantly lower risk of at least one unsuppressed HIV RNA (≥200 copies/mL) over the 15-month follow-up. There were concurrent, statistically significant intervention-related increases in positive affect as well as decreases in the self-reported frequency of stimulant use at six and twelve months.

Conclusions: Delivering a positive affect intervention during community-based CM with sexual minority men who use methamphetamine achieved durable and clinically meaningful reductions in HIV viral load that were paralleled by increases in positive affect and decreases in stimulant use. Further clinical research is needed to determine the effectiveness of integrative, behavioural interventions for optimizing the clinical and public health benefits of TasP in sexual minority men who use stimulants such as methamphetamine.
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http://dx.doi.org/10.1002/jia2.25436DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6924317PMC
December 2019

Pilot Randomized Controlled Trial of a Syndemics Intervention with HIV-Positive, Cocaine-Using Women.

AIDS Behav 2019 Sep;23(9):2467-2476

Department of Public Health Sciences, School of Medicine, University of Miami, Miami, USA.

This pilot randomized controlled trial examined the feasibility and acceptability of a Syndemics intervention targeting the intersection of stimulant use, trauma, and difficulties with HIV disease management in cocaine-using women. All participants received contingency management (CM) for 3 months with financial incentives for stimulant abstinence during thrice-weekly urine screening and refilling antiretroviral medications monthly. Sixteen participants were randomized to complete four expressive writing (n = 9) or four neutral writing (n = 7) sessions delivered during the CM intervention period. Completion rates for writing sessions were high (15 of 16 women completed all four sessions) and engagement in CM urine screening was moderate with women randomized to expressive writing providing a median of 11 non-reactive urine samples for stimulants. There were non-significant trends for those randomized to expressive writing to provide more CM urine samples that were non-reactive for stimulants, report greater decreases in severity of cocaine use, and display reductions in log HIV viral load at 6 months. Although the Syndemics intervention was feasible and acceptable to many women, qualitative interviews with eligible participants who were not randomized identified structural and psychological barriers to engagement. Further clinical research is needed to test the efficacy of Syndemics interventions with HIV-positive, cocaine-using women.
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http://dx.doi.org/10.1007/s10461-019-02625-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6880306PMC
September 2019

Housing First: Unsuppressed Viral Load Among Women Living with HIV in San Francisco.

AIDS Behav 2019 Sep;23(9):2326-2336

Department of Public Health Sciences, University of Miami, Miami, FL, USA.

While poverty is an established barrier to achieving success at each step of the HIV care continuum, less is known about specific aspects of poverty and how they overlap with behavior in exceptionally low-income individuals who live in well-resourced areas. We considered unsuppressed viral load over 3 years among women living with HIV in San Francisco who used homeless shelters, low-income hotels and free meal programs. One-hundred twenty study participants were followed; 60% had > 1 unsuppressed viral load and 19% were unsuppressed at every visit. Across six-month intervals, the odds of unsuppressed viral load were 11% higher for every 10 nights spent sleeping on the street [Adjusted Odds Ratio (AOR) 1.11, 95% CI 1.02-1.20]; 16% higher for every 10 nights spent sleeping in a shelter (AOR/10 nights 1.16, 95% CI 1.06-1.27); 4% higher for every 10 nights spent sleeping in a single-room occupancy hotel (AOR/10 nights 1.04, 95% CI 1.02-1.07); and over threefold higher among women who experienced any recent incarceration (AOR 3.56, 95% CI 1.84-6.86). Violence and recent use of outpatient health care did not significantly predict viral suppression in adjusted analysis. While strategies to promote retention in care are important for vulnerable persons living with HIV, they are insufficient to ensure sustained viral suppression in low-income women experiencing homelessness and incarceration. Results presented here in combination with prior research linking incarceration to homelessness among women indicate that tailored interventions, which not only consider but prioritize affordable housing, are critical to achieving sustained viral suppression in low-income women living with HIV.
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http://dx.doi.org/10.1007/s10461-019-02601-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7478361PMC
September 2019

Brief Report: Hazardous Cannabis Use and Monocyte Activation Among Methamphetamine Users With Treated HIV Infection.

J Acquir Immune Defic Syndr 2019 07;81(3):361-364

School of Medicine, University of Miami, Miami, FL.

Background: The use of stimulants, such as methamphetamine, has been associated with greater immune activation in treated HIV infection. However, relatively little is known about whether concomitant cannabis use is associated with lower immune activation among HIV-positive stimulant users.

Setting: HIV-positive, sexual minority men with biologically confirmed, recent methamphetamine use were enrolled in San Francisco, CA.

Methods: In total, 78 methamphetamine-using sexual minority men with an undetectable HIV viral load (<40 copies/mL) completed self-report measures of cannabis use and substance use disorder severity. Plasma biomarkers of monocyte activation (ie, sCD14 and sCD163) and intestinal barrier integrity (iFABP) were measured. The associations of hazardous cannabis use with these measurements were examined after adjusting for substance use disorder severity, age, antiretroviral therapy regimen, CD4 T-cell count, and interleukin-6.

Results: Hazardous cannabis users had the highest mean sCD14 levels (2181 ng/mL) compared with nonhazardous users (1991 ng/mL) and nonusers (1859 ng/mL; P = 0.05). In adjusted analyses, greater cannabis use severity was associated with higher sCD14 compared with nonusers (unstandardized beta = 133.6 ng/mL, P = 0.03). Cannabis use severity was not significantly associated with sCD163 or iFABP.

Conclusions: Hazardous cannabis use is independently associated with elevations in a clinically relevant marker of immune activation in methamphetamine users with treated HIV.
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http://dx.doi.org/10.1097/QAI.0000000000002046DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6613827PMC
July 2019

Detecting Disengagement From HIV Care Before It Is Too Late: Development and Preliminary Validation of a Novel Index of Engagement in HIV Care.

J Acquir Immune Defic Syndr 2019 06;81(2):145-152

Department of Medicine, Zuckerberg San Francisco General Hospital, University of California, San Francisco, San Francisco, CA.

Background: Engagement in care is critical to achieving and sustaining optimal benefits of efficacious antiretroviral therapies for HIV infection. Current metrics of engagement in care, including problematic patterns of retention in care, adherence to treatment, and viral suppression, are often detected late in the disengagement process. We sought to develop and validate a patient-centered screener of engagement in care that can be used to identify deficits in patient perceptions of engagement before the development of poor outcomes, including loss to follow-up, treatment nonadherence, virologic failure, and the resulting increased likelihood of HIV-associated morbidity and mortality and onward transmission of HIV.

Setting And Methods: Using input from patients, providers, and researchers through in-person focus groups and an online Delphi process, we developed a self-report measure of engagement in care that was validated with 3296 patients from 7 clinics across the United States.

Results: Results supported a single dimension of engagement in care measured by 10 items. Lower scores on the HIV Index were related to higher depression and anxiety symptoms, greater use of alcohol and stimulants, and increased likelihood of reporting internalized HIV stigma. Higher Index scores were positively associated with self-report measures of antiretroviral therapy adherence, corroborative clinic records documenting appointment attendance, and increased likelihood of recent viral load suppression.

Conclusions: The HIV Index offers promise as a patient-centered diagnostic and prognostic screener for engagement in care that can be used to trigger interventions to promote better clinical outcomes for persons living with HIV.
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http://dx.doi.org/10.1097/QAI.0000000000002000DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6522296PMC
June 2019

Stimulant Use and Viral Suppression in the Era of Universal Antiretroviral Therapy.

J Acquir Immune Defic Syndr 2019 01;80(1):89-93

Department of Medicine, University of California, San Francisco School of Medicine, San Francisco, CA.

Background: HIV-positive persons who use stimulants such as methamphetamine experience difficulties navigating the HIV care continuum that undermine the benefits of antiretroviral therapy (ART). However, few studies have examined the association of stimulant use with viral suppression in the era of universal ART.

Setting: Zuckerberg San Francisco General Hospital.

Methods: HIV-positive persons participating in a clinical cohort study and taking ART completed assessments every 4-6 months. The exposure was the cumulative, time-varying proportion of assessments with any self-reported stimulant use. The time-varying outcome, HIV viral suppression (ie, <200 copies/mL), was measured at assessments or extracted from the clinical record.

Results: In total, 1635 HIV-positive participants on ART contributed 17,610 person-visits over a median of 2.3 [interquartile range (IQR) = 1.0-5.3] years of follow-up. Participants were middle-aged (median = 45.0; IQR = 38.0-52.0), predominantly white (57%), sexual minority men (78%), with a median CD4 T-cell count of 409 (IQR = 225-640) cells/mm at enrollment. Significant increases in odds of viral suppression over time were less pronounced among stimulant users compared with nonusers, particularly before the advent of universal ART. Increasing odds of viral suppression were paralleled by declining stimulant use over time. In the universal ART era, increasing odds of viral suppression were observed at lower levels of stimulant use, but not when participants reported using stimulants at every visit.

Conclusions: Although ART benefits are still not achieved as rapidly in stimulant users, this disparity is not as large in the era of universal ART.
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http://dx.doi.org/10.1097/QAI.0000000000001867DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6289664PMC
January 2019

Over the influence: The HIV care continuum among methamphetamine-using men who have sex with men.

Drug Alcohol Depend 2018 11 13;192:125-128. Epub 2018 Sep 13.

School of Medicine, University of California - San Francisco, 1600 Divisadero St., San Francisco, CA 94115 USA; Department of Public Health Sciences, University of Miami, 1120 NW 14th St., Office 1005, Miami, FL 33136 USA. Electronic address:

Background: HIV-positive persons who use stimulants such as methamphetamine experience greater difficulties in navigating the HIV care continuum. In the era of HIV treatment as prevention (TasP), little is known about the prevalence and correlates of success along the HIV care continuum among people who use stimulants.

Setting: San Francisco, California USA METHODS: Cross-sectional study that enrolled 129 HIV-positive men who have sex with men (MSM) from 2013 through 2017 who had biologically confirmed, recent methamphetamine use. Multivariable logistic regressions were built to identify correlates of success across the HIV care continuum.

Results: Although two-thirds (87/129) of participants had undetectable HIV viral load (<40 copies/mL), only one-in-four (32/129) reported taking at least 90% of their antiretroviral therapy (ART). Those who were homeless in the past year (adjusted odds ratio [aOR] = 0.20; 95% CI = 0.06-0.65) had 80% lower odds of being undetectable and adherent to ART. Substance use disorder treatment was associated with 77% lower odds of being engaged in HIV care (aOR = 0.23; 95% CI = 0.06-0.84) but also close to 3-fold greater odds of being adherent to ART (aOR = 2.91; 95% CI = 1.12-7.60).

Conclusion: Despite the fact that many HIV-positive, methamphetamine-using MSM are able to achieve undetectable viral load in this sample, difficulties with ART adherence threaten to undermine the clinical and public health benefits of TasP. Expanded efforts to boost the effectiveness of TasP in this population should focus on meeting the unique needs of homeless individuals, optimizing ART adherence, and facilitating the integration of HIV care with substance use disorder treatment.
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http://dx.doi.org/10.1016/j.drugalcdep.2018.07.038DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6612057PMC
November 2018

Randomized controlled trial of a positive affect intervention for methamphetamine users.

Drug Alcohol Depend 2018 11 5;192:8-15. Epub 2018 Sep 5.

Department of Medical Social Sciences, Feinberg School of Medicine, Northwestern University, 633 N. Saint Clair St., 19th Floor, Chicago, IL 60611 USA.

Background: Contingency management (CM) is an evidence-based intervention providing rewards in exchange for biomarkers that confirm abstinence from stimulants such as methamphetamine. We tested the efficacy of a positive affect intervention designed to boost the effectiveness of CM with HIV-positive, methamphetamine-using sexual minority men.

Methods: This attention-matched, randomized controlled trial of a positive affect intervention delivered during CM was registered on www.clinicaltrials.gov (NCT01926184). In total, 110 HIV-positive sexual minority men with biologically confirmed, recent methamphetamine use were enrolled. Five individual sessions of a positive affect intervention (n = 55) or an attention-control condition (n = 55) were delivered during three months of CM. Secondary outcomes examined over the 3-month intervention period included: 1) psychological processes relevant to affect regulation (i.e., positive affect, negative affect, and mindfulness); 2) methamphetamine craving; 3) self-reported stimulant use (past 3 months); and 4) cumulative number of urine samples that were non-reactive for stimulants (i.e., methamphetamine and cocaine) during CM.

Results: Those randomized to the positive affect intervention reported significant increases in positive affect during individual sessions and increases in mindfulness over the 3-month intervention period. Intervention-related improvements in these psychological processes relevant to affect regulation were paralleled by concurrent decreases in methamphetamine craving and self-reported stimulant use over the 3-month intervention period.

Conclusions: Delivering a positive affect intervention may improve affect regulation as well as reduce methamphetamine craving and stimulant use during CM with HIV-positive, methamphetamine-using sexual minority men.
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http://dx.doi.org/10.1016/j.drugalcdep.2018.07.029DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6200638PMC
November 2018

Psychosocial Correlates of Monocyte Activation and HIV Persistence in Methamphetamine Users.

J Neuroimmune Pharmacol 2019 03 25;14(1):16-22. Epub 2018 Jul 25.

School of Medicine, University of Miami, Miami, FL, USA.

This cross-sectional study investigated the associations of psychosocial factors relevant to recovery from substance use disorders with monocyte activation and HIV persistence in a sample of 84 HIV-positive, methamphetamine-using sexual minority men with undetectable HIV viral load (<40 copies/mL). We examined if psychosocial factors were associated with decreased soluble CD14 (sCD14) and lower proviral HIV DNA. Multiple linear regression models adjusted for age, anti-retroviral therapy regimen, and CD4+ T-cell count. Time on ART was also included in models examining proviral HIV DNA. Greater self-efficacy for managing methamphetamine triggers and higher social support for abstinence were independently associated with lower sCD14. Greater social support for abstinence was also independently associated with lower proviral HIV DNA. Psychosocial factors relevant to recovery from substance use disorders are associated with lower monocyte activation and decreased proviral HIV DNA. Findings underscore the need for longitudinal research to identify plausible mechanisms linking psychosocial factors and substance use with biological processes relevant to HIV pathogenesis.
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http://dx.doi.org/10.1007/s11481-018-9797-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6347547PMC
March 2019

Optimizing Contingency Management with Methamphetamine-Using Men who Have Sex with Men.

Cogn Behav Pract 2018 May 11;25(2):286-295. Epub 2017 Sep 11.

University of Miami School of Medicine, Department of Public Health Sciences.

Among men who have sex with men (MSM), methamphetamine use is associated with multiple, overlapping syndemic conditions including increased risk for HIV seroconversion and onward HIV transmission. Contingency management (CM) is an evidence-based, behavioral intervention implemented to curb methamphetamine use and optimize HIV/AIDS prevention among MSM in San Francisco since 2003. We conducted a program evaluation to document the evolution of this 12-week CM program to include delivery of brief, individual counseling incorporating motivational interviewing and behavioral skills. A drop-in group delivered concurrently with CM urine-screening visits also provides peer support as well as referrals for other social and medical services. From December 2011-October 2013, a total of 131 clients enrolled in the CM program and provided a median of 22 urine samples (Interquartile Range = 10-34) that were non-reactive for methamphetamine. Findings support the feasibility and acceptability of integrating individual and group counseling with community-based CM for methamphetamine-using MSM.
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http://dx.doi.org/10.1016/j.cbpra.2017.08.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7252223PMC
May 2018

Recent stimulant use and leukocyte gene expression in methamphetamine users with treated HIV infection.

Brain Behav Immun 2018 07 18;71:108-115. Epub 2018 Apr 18.

New York University College of Dentistry Bluestone Center for Clinical Research, United States.

Stimulant use may accelerate HIV disease progression through biological and behavioral pathways. However, scant research with treated HIV-positive persons has examined stimulant-associated alterations in pathophysiologic processes relevant to HIV pathogenesis. In a sample of 55 HIV-positive, methamphetamine-using sexual minority men with a viral load less than 200 copies/mL, we conducted RNA sequencing to examine patterns of leukocyte gene expression in participants who had a urine sample that was reactive for stimulants (n = 27) as compared to those who tested non-reactive (n = 28). Results indicated differential expression of 32 genes and perturbation of 168 pathways in recent stimulant users. We observed statistically significant differential expression of single genes previously associated with HIV latency, cell cycle regulation, and immune activation in recent stimulant users (false discovery rate p < 0.10). Pathway analyses indicated enrichment for genes associated with inflammation, innate immune activation, neuroendocrine hormone regulation, and neurotransmitter synthesis. Recent stimulant users displayed concurrent elevations in plasma levels of tumor necrosis factor - alpha (TNF-α) but not interleukin 6 (IL-6). Further research is needed to examine the bio-behavioral mechanisms whereby stimulant use may contribute to HIV persistence and disease progression.
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http://dx.doi.org/10.1016/j.bbi.2018.04.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6003871PMC
July 2018

Substance-associated elevations in monocyte activation among methamphetamine users with treated HIV infection.

AIDS 2018 03;32(6):767-771

University of Miami School of Medicine, Miami, Florida.

Objective: Microbial translocation and monocyte activation predict mortality in treated HIV. We examined whether substance use independently contributes to these pathophysiologic processes.

Design: Cross-sectional study at baseline for a randomized controlled trial.

Methods: HIV-positive, methamphetamine-using MSM with undetectable HIV viral load (less than 40 copies/ml) were enrolled. We examined if plasma biomarkers of monocyte activation and intestinal barrier integrity were associated with the following: reactive urine toxicology results (Tox+) for stimulants (i.e., methamphetamine or cocaine) and substance use severity measured by the Addiction Severity Index. Multiple linear regression models adjusted for age, antiretroviral therapy regimen, CD4 T-cell count, interleukin-6, and alcohol use severity.

Results: The sample of 84 virally suppressed MSM had a median CD4 T-cell count of 645 cells/μl. Those who were Tox+ for stimulants displayed higher soluble CD14 (sCD14) levels (2087 versus 1801 ng/ml; P = 0.009), and this difference remained significant after adjusting for covariates (standardized beta = 0.23, P = 0.026). Greater substance use severity was also independently associated with higher sCD14 after adjusting for covariates (standardized beta = 0.29, P = 0.013). Being Tox+ for stimulants and substance use severity were not associated with soluble CD163 (sCD163) or intestinal fatty acid binding protein (iFABP) levels (P > 0.05).

Conclusions: Monocyte activation is one plausible mechanism by which stimulant use may increase clinical HIV progression.
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http://dx.doi.org/10.1097/QAD.0000000000001751DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5912167PMC
March 2018

A longitudinal study of persistent smoking among HIV-positive gay and bisexual men in primary relationships.

Addict Behav 2017 03 18;66:118-124. Epub 2016 Nov 18.

Department of Medicine, University of California, San Francisco, USA.

Introduction: We examined the stability of smoking behaviors, and factors associated with persistent smoking in a longitudinal study of HIV-positive gay and bisexual men in primary relationships.

Methods: A sample of 377 HIV-positive men on antiretroviral therapy and their same-sex partners completed five assessments over two years. Participants completed semi-structured interviews which assessed smoking status, sociodemographic factors, relationship dynamics, and HIV-related disease characteristics. Latent transition analysis estimated the amount of transition in smoking over time. Latent class analysis examined factors associated with smoking status across the study period.

Results: At baseline, 28.1% (n=106) of participants reported current smoking. Over 90% of the HIV-positive men remained in the same smoking category over time (68.4% persistent non-smokers; 24.1% persistent smokers). Men whose partners smoked and men with lower income had higher odds of being persistent smokers, whereas older men and men who identified as Latino race/ethnicity had lower odds of being persistent smokers compared to non-smokers.

Conclusions: Despite efforts to reduce smoking among people living with HIV (PLWH), a substantial subset of men continued to smoke during their two years in the study. Findings suggest that primary partners who also smoke and low income were the strongest predictors of sustained smoking behaviors among HIV-positive men. Additional research is needed to better understand how to increase motivation and support for smoking cessation among PLWH and their primary partners, while attending to how socioeconomic status may inhibit access to and the sustained impact of existing smoking cessation programs.
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http://dx.doi.org/10.1016/j.addbeh.2016.11.019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5525143PMC
March 2017

A community-engaged randomized controlled trial of an integrative intervention with HIV-positive, methamphetamine-using men who have sex with men.

BMC Public Health 2016 07 30;16:673. Epub 2016 Jul 30.

Department of Medical Social Sciences, Northwestern University, San Francisco, USA.

Background: Contingency management (CM) is an evidence-based intervention providing tangible rewards as positive reinforcement for abstinence from stimulants such as methamphetamine. Integrative approaches targeting affect regulation could boost the effectiveness of CM in community-based settings and optimize HIV/AIDS prevention efforts.

Methods/design: This randomized controlled trial with HIV-positive, methamphetamine-using men who have sex with men (MSM) is examining the efficacy of a 5-session, individually delivered positive affect regulation intervention - Affect Regulation Treatment to Enhance Methamphetamine Intervention Success (ARTEMIS). ARTEMIS is designed to sensitize individuals to non-drug-related sources of reward as well as assist with managing depression and other symptoms of stimulant withdrawal during CM. HIV-positive, methamphetamine-using MSM who are enrolled in a community-based, 12-week CM program are randomized to receive ARTEMIS or an attention-matched control condition. Follow-up assessments are conducted at 3, 6, 12, and 15 months after enrollment in CM. Four peripheral venous blood samples are collected over the 15-month follow-up with specimen banking for planned biomarker sub-studies. The primary outcome is mean HIV viral load. Secondary outcomes include: sustained HIV viral suppression, T-helper cell count, psychological adjustment, stimulant use, and potentially amplified transmission risk behavior.

Discussion: Implementation of this randomized controlled trial highlights the importance of delineating boundaries between research activities and community-based service provision. It also provides insights into best practices for integrating the distinct agendas of academic and community partners in clinical research. This trial is currently enrolling and data collection is anticipated to be completed in September of 2018.

Trial Registration: This trial was registered on clinicaltrials.gov ( NCT01926184 ) on August 16, 2013.
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http://dx.doi.org/10.1186/s12889-016-3325-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4967339PMC
July 2016
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