JAIDS Journal of Acquired Immune Deficiency Syndromes:
Participant Characteristics and HIV Risk Behaviors Among Individuals Entering Integrated Buprenorphine/Naloxone and HIV Care
Chaudhry, Amina A MD, MPH*; Botsko, Michael MSW, MPhil†; Weiss, Linda PhD‡; Egan, James E MPH‡; Mitty, Jennifer MD§; Estrada, Barbara MS‖; Lucas, Gregory M MD, PhD*; Woodson, Tanita MA, NP*; Flanigan, Timothy P MD**; Fiellin, David A MD††; for the BHIVES Collaborative
From the *Johns Hopkins University, Baltimore, MD; †Center for HIV Educational Studies and Training, New York, NY; ‡New York Academy of Medicine, New York, NY; §Beth Israel Deaconess Medical Center, Boston, MA; ‖Impact Consultants, Inc, Tucson, AZ; **Brown University School of Medicine, Providence, RI; ††Yale University School of Medicine, New Haven, CT; and ‡‡The CORE Center (Chicago, IL), El Rio Santa Cruz Neighborhood Health Center (Tucson, AZ), Johns Hopkins University (Baltimore, MD), Miriam Hospital (Providence, RI), Montefiore Medical Center (Bronx, NY), OASIS (Oakland, CA), Oregon Health Sciences University (Portland, OR), University of California San Francisco Positive Health Program at San Francisco General Hospital (San Francisco, CA), University of Miami Medical School (Miami, FL), Yale University School of Medicine (New Haven, CT), and The New York Academy of Medicine (New York, NY).
This initiative was funded by the US Health and Human Services/Health Resources and Services Administration grant number H97HA03793.
The authors have no conflicts of interest to disclose.
Correspondence to: Amina A. Chaudhry, MD, MPH, Assistant Professor of Medicine, Johns Hopkins Bayview Medical Center, MFL Building, West Tower, Room 528, 5200 Eastern Avenue, Baltimore, MD 21224 (e-mail: firstname.lastname@example.org).
Objective: This study was part of a national, multisite demonstration project evaluating the impact of integrated buprenorphine/naloxone treatment and HIV care. The goals of this study were to describe the baseline demographic, clinical, and substance use characteristics of the participants and to explore HIV transmission risk behaviors in this group.
Methods: Nine sites across the United States participated. Data obtained by interview and chart review included demographic information, medical history, substance use, and risk behaviors.We performed a descriptive analysis of patient characteristics at entry and used logistic regression to evaluate factors associated with 1) unprotected anal or vaginal sex; and 2) needle-sharing within the previous 90 days.
Results: Three hundred eighty-six individuals were included in the study: 303 (78.5%) received buprenorphine/naloxone; 41 (10.6%) received methadone; and 42 (10.9%) received another form of treatment. The analysis of risk behaviors was limited to those in the buprenorphine group (n = 303). Among those reporting vaginal or anal sex in the previous 90 days, 24% had sex without a condom. Factors significantly associated with unprotected sex were: having a partner; female gender; and alcohol use in previous 30 days. A total of 8.9% of participants shared needles in the previous 90 days. Factors significantly associated with needle-sharing were: amphetamine use; marijuana use; homelessness; and anxiety.
Conclusions: Addressing transmission risk behaviors is an important secondary HIV prevention strategy. In addition to treatment for opioid dependence, addressing other substance use, social issues, particularly housing, and mental health may have important implications for reducing HIV transmission in HIV-infected opioid-dependent patients.
Opioid dependence in the United States exerts a substantial public burden with devastating health, social, and economic consequences. In 2009, over 1.8 million Americans aged 12 years and older met criteria for abuse and dependence on analgesics, and 399,000 met criteria for abuse or dependence on heroin.1 According to the Drug Abuse Warning Network, in 2006, approximately 324,000 emergency department visits in the United States involved the nonmedical use of pain relievers, mostly opioid analgesics.2 Health consequences of illicit opioid use include the risk of overdose3 and risks associated with mode of drug use, particularly injection drug use (IDU).
Treatment of opioid dependence with opioid agonist therapy (ie, methadone or buprenorphine) has been demonstrated to be effective in numerous studies.4-9 Despite effective pharmacotherapy, patient access to medication-assisted treatment (MAT) for opioid dependence remains limited. In the United States in 2007, only 29% of persons entering treatment for heroin and 20% of those entering treatment for other opioids received MAT with opioid agonist treatment.10 Before 2002, MAT for opioid dependence treatment in the United States had generally been restricted to federally regulated treatment programs offering methadone. The US Food and Drug Administration approval of buprenorphine in 2002 offered a new treatment option with the potential for increasing treatment capacity and opened up the opportunity for integration of opioid dependence treatment into general medical care. Available evidence suggests that integration of mental health and primary care may led to improved access to care,11 quality of care,12,13 better health-related quality of life,12 and may be cost-neutral.13-15 Further research on the integration of treatment for substance use disorders and general medical care is needed to fully understand the benefits and cost-effectiveness of integrated care.
The epidemics of HIV and substance-related disorders have been closely linked since the early days of the HIV epidemic, when IDU was first recognized as a major risk factor for HIV transmission. Data from the Centers for Disease Control and Prevention (CDC) estimate that by the end of 2006, IDU accounted for 18.5% of prevalent cases of HIV; 5.0% of persons living with HIV reported both male-to-male sexual contact and IDU.16 Furthermore, among persons living with HIV/AIDS, active drug and alcohol use has been shown to be: a barrier to treatment adherence17-22; a barrier to healthcare use including receipt of antiretrovirals23,24; and associated with inadequate viral suppression.21,25-27
A recent systematic review demonstrated that opioid agonist treatment reduces both injection-related and sexual HIV risk behaviors among injection drug users.28 Methadone maintenance treatment has been demonstrated to decrease HIV seroconversion.29,30 Buprenorphine treatment in a primary care setting has also been found to reduce drug-related HIV transmission risk behaviors.31 Thus, addressing opioid use through MAT has important implications for HIV treatment and health outcomes for HIV-infected individuals as well as in secondary prevention of HIV infection.
The availability of buprenorphine offered an important new integration opportunity for HIV care providers and an opportunity to improve HIV-related health outcomes as well as risk behaviors. Previous studies providing HIV treatment on-site in methadone treatment programs have demonstrated improvements in adherence to HIV medication32 and viral suppression.33,34 Buprenorphine offers the option of bringing MAT for opioid dependence into the HIV clinic. Sullivan et al demonstrated that implementation of office-based buprenorphine in an HIV medical practice was feasible and demonstrated a high rate of retention in integrated buprenorphine/HIV care.35
Recognizing the potential for delivery of novel models of care integrating HIV and opioid-dependence treatment, the Health Resources and Services Administration's HIV/AIDS bureau supported the development of demonstration projects integrating buprenorphine/naloxone (bup/nx) treatment into HIV primary care settings under the Special Projects of National Significance program, which works to advance delivery of health and support services to underserved populations with HIV. Ten sites across the United States were chosen to take part in this national, multisite demonstration project implementation and its evaluation, including the impact of integrated care on HIV outcomes, substance use outcomes, mental health, quality of care, and more.
The current study focuses on the participants at the time of entry into treatment in the demonstration programs. It includes a descriptive analysis of participants at the baseline assessment. The specific goals of this study were to describe the demographic, clinical, and substance-related characteristics of the participants and to explore HIV transmission risk behaviors in this group. Specifically, we sought to identify factors associated with 1) unprotected anal or vaginal sex; and 2) needle-sharing 90 days.
As described more fully in this supplement36,37 from 2004 to 2009, the HIV/AIDS Bureau of the Health Resources and Services Administration funded, through its Special Projects of National Significance, the development of demonstration programs that integrated HIV care and bup/nx treatment for opioid dependence at 10 sites across the United States. The Health Resources and Services Administration also funded an Evaluation and Technical Assistance Center (the “Center”) to coordinate the multisite mixed-method evaluation, provide clinical and evaluation support and technical assistance, and promote dissemination of findings. Data from nine of the 10 sites were included in the multisite evaluation.
These sites were scattered across the United States, primarily concentrated on the coasts, and included both community health centers and university-based clinics. Each site designed its own integrated HIV care/bup/nx intervention, offering medical management of bup/nx treatment, counseling, and linkage to supportive services. A detailed description of the models of care at each of the sites is beyond the scope of this article; it is reviewed elsewhere in this supplement.38
We conducted a cross-sectional analysis of data collected at the baseline assessment. Six sites used a trained interviewer to administer the baseline survey, and three sites (Johns Hopkins, Montefiore Medical Center, and El Rio Neighborhood Health Center) used an audio computer-assisted interview format, which was supported (in case of questions) by on-site research personnel. Data ascertained by survey included demographic information, education, employment, housing status, HIV disease history including likely mode of transmission, symptom distress, antiretroviral use and adherence, other medical history, substance use characteristics, including treatment history, and history of recent HIV transmission risk behaviors, including having had vaginal or anal sex without a condom and both receptive and distributive sharing of needles or other injection-related items. Validated instruments incorporated into the assessment included the Addiction Severity Index-Lite.39 Brief Symptom Inventory,40 SF-12,41 and Center for Epidemiologic Studies Depression Scale.42
Additionally, data were obtained by chart review using standardized chart abstraction forms. Data obtained from chart review included year of HIV diagnosis, CD4 lymphocyte count (most recent and nadir) most recent HIV RNA, antiretroviral use including regimen, hepatitis B and C serology, most recent transaminases, AIDS-defining illnesses in the past 6 months, and use of MAT at baseline.
We performed a descriptive analysis of patient characteristics, including substance use history among all participants; among those patients receiving buprenorphine, we evaluated factors associated with two HIV transmission risk behaviors: unprotected anal or vaginal sex and needle-sharing.
We generated summary statistics for demographic, clinical, social, and substance use characteristics. To assess factors associated with HIV transmission risk behaviors at baseline (needle-sharing and unprotected anal or vaginal sex within the previous 90 days), we conducted bivariate analyses using partial least squared or logistic regression models. We constructed multivariate models that included all covariates with relationships at the P < 0.1 level in bivariate analysis and then developed the most parsimonious multivariate model.
Because each site designed its own study and method of allocating patients to treatment options (random versus by patient choice), intervention and comparison groups were not uniform across sites. Consistent with the approach taken for other cross-site analyses, we categorized participants into three treatment strategies: integrated bup/nx, methadone, or other treatment.37 For our descriptive analysis, we performed chi-square tests comparing the characteristics among the different treatment groups. For the analysis of unprotected sex, we excluded individuals who reported not having had sex in the previous 90 days.
Three hundred eighty-six individuals were included in the analysis of participant characteristics: 303 received bup/nx, 41 received methadone, and 42 received some other form of treatment. Only the buprenorphine group was included in the analysis of risk behaviors. As displayed in Table 1, the sample was approximately two thirds male. Although 56% of the overall sample was black, 85% of those in the “other treatment” group were black compared with 52% in the bup/nx group and 56% in the methadone group. The mean age was 45.6 years (standard deviation, 7.9); almost half of the participants were aged 40 to 49 years at study enrollment. Approximately half of participants had never been married, and 16% were married or partnered. Eighty-three percent of participants reported their sexual orientation as straight, 9% as gay or lesbian, and 8% as bisexual. Forty-four percent of participants had less than a high school education, 34% had a high school diploma or equivalent, and 23% had at least some college. Seventy-five percent were unemployed at the time of entry into the study and 25% were homeless. The majority (79%) had been in jail for more than 3 days at least once, and 28% were on parole or probation at the time of entry to the study.
HIV and Other Medical Characteristics
Approximately half of participants reported IDU as their transmission category, and 81% had been diagnosed 5 or more years before entry into the study with a mean time since HIV diagnosis of 12.0 years (standard deviation, 6.4). Forty-nine percent had a CD4 nadir of less than 200 by chart abstraction and just 9% had an AIDS-defining illness in the previous 6 months. Sixty-one percent were receiving highly-active antiretroviral therapy (HAART). Approximately one fourth (26%) of those on HAART reported missing at least one dose within the previous week. Of those with available test results (n = 271), 7% were hepatitis B surface antigen-positive; of 299 with hepatitis C antibody testing results available, 81% were positive.
Substance use (lifetime and past month) characteristics are summarized in Figure 1. Past month substance use by treatment group is displayed in Figure 2. Forty-seven percent had been in some form of treatment in the 90 days before their initial study assessment, including 22% who had been on methadone. The vast majority (90%) reported no previous receipt of buprenorphine.
Unprotected Anal or Vaginal Sex
Among participants reporting having had vaginal or anal sex in the previous 90 days, 24% reported having had sex without a condom (Table 2).
In the bivariate analysis, factors associated with unprotected anal or vaginal sex in the previous 90 days at the P < 0.10 significance level to be included in the multivariate analysis were: female gender, being partnered or married, race/ethnicity, past 30-day alcohol use, past 30-day heroin use, and hepatitis B surface antibody positivity (data not shown). Age, having some college, lifetime history of alcohol use, lifetime history of nonheroin opiates, hepatitis B core antibody positivity, and being on HAART were inversely associated with unprotected sex (P < 0.10 level) in the bivariate analysis (data not shown). In multivariate analysis, having a partner, female gender, and alcohol use in past 30 days were significantly associated with unprotected sex. Lifetime history of nonheroin opiate use and HAART use each demonstrated an inverse association with unprotected sex (Table 3).
We found that 8.9% of overall participants reported sharing needles in the previous 90 days (Table 2). In the bivariate analyses, sexual orientation; homelessness; past 30-day heroin, cocaine, amphetamine, and marijuana use; lifetime alcohol and amphetamine use; Addiction Severity Index-Lite alcohol and drug scores; HIV symptom distress score; Brief Symptom Inventory anxiety score; and Center for Epidemiologic Studies Depression Scale score were significantly associated with needle sharing at the P < 0.1 level (data not shown). Factors in the bivariate analysis that were inversely related to needle-sharing at the P < 0.1 level were: SF-12 general health, social functioning, role emotional, and mental health scores, and current HAART use. In the parsimonious multivariate analysis, factors associated with needle-sharing were: past 30-day amphetamine use, past 30-day amphetamine use, homelessness, and BSI anxiety score (Table 4).
Our findings provide a cross-sectional view of treatment-seeking HIV-infected opioid-dependent patients across the United States, encompassing diverse geographic and clinical settings as well as a range of treatment models. We identified several key findings in patient characteristics that will generate additional research directions and may help guide program development. In terms of substance use, over half of these opioid-dependent individuals reported using cocaine in the previous month, and approximately half reported alcohol consumption in the previous month. We also found that a substantial portion of study participants engaged in recent HIV transmission risk behaviors. This is salient because in general, these participants were engaged in HIV care, suggesting that attention to transmission risk behaviors is an area that needs continual attention from HIV care providers, addiction treatment providers, and researchers.
Our data suggest that among these opioid-dependent individuals, other substance use, principally cocaine and alcohol, is common. Cocaine use in our study population is discussed in detail elsewhere in this supplement.43 Alcohol use among persons with HIV is associated with poorer adherence,44,45 lower rates of viral suppression21,25,26 and HIV progression.26 Among those who use illicit drugs, studies suggest that those using stimulants, including cocaine and crack, may be least likely to access care46,47 and when in care tend to have poorer adherence to treatment.18,20
These data highlight the need for comprehensive assessment and treatment for other substances in addition to opioids, including alcohol, which almost half of participants reported using in the past month. This is an important issue for office-based treatment programs that might not have resources available on-site for managing other substance use. Facilitated linkage and referral to other treatment services may be important in addressing multisubstance use. Still, effective behavioral and pharmacologic therapies for risky alcohol use exist, and the evidence has shown that brief interventions in healthcare settings can help decrease alcohol consumption in some patients not seeking alcohol treatment.48 One study found that a low-cost HIV primary care alcohol intervention was effective and could be sustained.49
Almost one fourth of those having sex reported having had anal or vaginal sex without a condom in the previous 90 days; 8.9% of overall participants reported sharing needles in the previous 90 days. A recent CDC study of data from the National HIV Behavioral Surveillance System50 found that in the prior 12 months: 32.8% of persons reporting IDU shared needles or syringes and 58.5% shared other injection-related equipment (such as “cookers” or rinse water); 63.4% engaged in unprotected vaginal intercourse and 47.8% reported multiple sex partners. In the same CDC study, 66.3% of IDUs were tested for HIV during the prior 12 months and 72.2% reported ever having been tested for or having a diagnosis of hepatitis C virus.50 Thus, the majority of these active drug users are interfacing with the health system, which affords an opportunity for risk reduction intervention. Our study participants had lower but still substantial rates of unprotected sex and needle-sharing. The reasons for this difference are not known but may reflect increased HIV transmission knowledge, fear of HIV transmission, or engagement in care for HIV or for substance abuse. Almost half of our participants had been in substance abuse treatment in the previous 90 days. Additionally, we did not limit our study to IDU.
Risk factors in our study for having unprotected sex included having a partner, female gender, and alcohol use in the previous 30 days. We did not collect data on the HIV serostatus of partners in this study. Further exploration of knowledge, attitudes, and behaviors of HIV-infected opioid-dependent women concerning condom use is warranted to understand the barriers to more regular condom use in the population. The relationship between substance use and sexual risk behaviors has been explored in many studies with mixed results. A number of studies have shown increased sexual risk behaviors associated with alcohol and drug use,51-55 whereas others have shown varied or negative results, particularly when the outcome of interest is condom use.56-61
In our study, HAART use had an inverse relationship with unprotected sex, suggesting that engagement in care may play a role in, or be a marker for, risk reduction. We also found that lifetime use of nonheroin opiates had an inverse relationship with unprotected sex.
Risk factors in our study for needle-sharing included other substance use, homelessness, and anxiety. Amphetamine use and marijuana use were each independently associated with needle-sharing. This again highlights the need for comprehensive treatment strategies that addresses mental health and substance use in addition to opioid use. Amphetamine use and marijuana use were the most strongly associated with needle-sharing; those who used amphetamines were almost five times as likely to share needles as those who did not. Amphetamine-type stimulants such as methamphetamine have been associated with sexual risk behaviors,62 but our study suggests that needle-sharing is also an important consideration among those who use Amphetamine-type stimulants. There is very little known about the relationship between cannabis and HIV transmission risk behaviors, but our study suggests that further exploration of this is warranted.
Our study also suggests that addressing mental health may play a role in reducing HIV transmission risk. In a prior study, Lyketsos et al studied patients entering into HIV care at one of our sites (Baltimore, MD) and found that 40% had a primary psychiatric diagnosis plus current or prior substance use disorder.63 Mental health has been identified as an important cofactor in adherence to HIV treatment.17,64 Other studies have demonstrated that having psychiatric disorder may be associated with virologic failure65 and AIDS-related mortality66 and that engagement in mental health services has been associated with increased survival.66 Thus, concomitant identification and management of both substance-related and primary psychiatric diagnoses is essential in this population with a high prevalence of co-occurring disorders and should be further explored in studies of the impact of substance use disorders on HIV disease and secondary transmission of HIV.
Twenty-five percent of study participants were homeless; homeless individuals had over four times the odds of needle-sharing compared with adequately housed individuals. It has been estimated that 10% to 20% of homeless persons abuse drugs actively67,68 with a lifetime prevalence ranging from 25% to 50% according to some estimates.69 One survey in New Haven, CT, found that 25% of homeless people identified drug use as the primary reason for their being homeless.70 A study of CDC data on behavioral surveillance in HIV-infected persons at 19 sites found that self-reported physical and mental health was worse among homeless persons and that homeless persons had lower CD4 counts, were less likely to have used HAART, and were less adherent to HAART.71 Homelessness also has been demonstrated to increase the risk for transactional sex and other risky sexual behavior.72-74
Limitations to this study include reliance on self-reported data collection. The use of audio computer-assisted interview at some sites helps ameliorate this issue, although some social desirability bias and recall bias is likely present. Second, we cannot make direct comparisons among treatment groups, because there was no uniform system of treatment assignment across sites, and participants were not randomized to treatment groups. Additionally, our analysis of risk behaviors was cross-sectional, limiting our ability to make causal inferences about relationships between factors and relationships. Finally, the study designs were heterogeneous across sites. This may be a limitation in terms of internal validity and interpretation of our analysis of risk behaviors; however, it may also be considered a strength of our study in terms of generalizability to real-world clinical situations.
Our demonstration program characterizing a diverse population of opioid-dependent, HIV-infected persons entering treatment at sites across the country is the first of its kind evaluating the impact of integrated bup/nx and HIV care on a wide range of health outcomes. This particular study offers insights into the characteristics and particular needs of this population. Our study demonstrates that addressing HIV risk behaviors among HIV-infected persons entering opioid agonist treatment is an important secondary HIV prevention strategy. Furthermore, in addition to treatment for opioid dependence, addressing other substance use, social issues-particularly stable housing-and mental health is critical in efforts to reduce HIV risk behaviors and may have important implications for reducing HIV transmission.
The BHIVES Collaborative, sites, and Principal Investigators: R. Finkelstein and D. Fiellin, K. Carmichael, D. Sylvestre, P. T. Korthuis, C. Cunningham, M. Fischl, University T. Flanigan, P. Lum, G. Lucas, J. Watts, R. Altice, L. Sullivan, and M. N. Gourevitch, (Chair, National Advisory Committee). For more information, go to HYPERLINK “http://www.bhives.org” www.bhives.org.
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