Preexposure prophylaxis (PrEP), a biomedical HIV prevention strategy that involves the use of antiretroviral medications by HIV-negative individuals to reduce their risk of acquiring HIV, is an effective and underused tool in our HIV prevention arsenal for persons who inject drugs (PWID). Results of the Bangkok Tenofovir Study showed a 49% reduction in HIV acquisition and up to 74% among those with highest adherence among PWID taking once daily PrEP.1 In 2014, the Centers for Disease Control and Prevention recommended emtricitabine/tenofovir disoproxil fumarate as PrEP for PWID.2 However, research and programs to bring PrEP to scale have yet to focus on PWID. Therefore, little knowledge exists to help address PrEP implementation challenges among PWID, a group representing only 3% of the US population but 6% of new HIV infections in 2015 and 36% of cumulative AIDS deaths.3
Few studies have evaluated the willingness and acceptability to use PrEP among PWID. Stein and colleagues4 found that knowledge of PrEP was extremely low (7.4%) among opioid injectors entering detoxification treatment, but close to half were willing to take a pill to reduce risk of HIV. Willingness was associated with HIV risk perception (greater among those who perceived themselves at some risk for acquiring HIV) and beliefs about PrEP effectiveness (greater among individuals who believed PrEP to be highly effective).4 Data from the Washington, DC arm of the 2012 National HIV Behavioral Surveillance survey and from Vancouver similarly found low levels of knowledge about an “anti-HIV medication” but generally positive attitudes.5,6
Taken together, these US and Canadian studies indicate that 35% to 47% of PWID are willing to take PrEP.4–6 However, little is known about how to best roll out PrEP in diverse PWID communities. One setting to potentially introduce and provide PrEP is at syringe exchange programs (SEPs). A primary purpose of SEPs is to provide harm reduction supplies, such as new injection equipment, to PWID to prevent the spread of blood-borne viruses, including HIV, and other complications of injection drug use such as skin and soft tissue infections. Some SEPs have successfully incorporated medical services and long-term monitoring of health conditions into their harm reduction services. When hepatitis B vaccinations, which requires 3 visits to complete the vaccination series, were introduced into SEP services, completion rates were 2.7-fold higher (83% vs. 31%) than those when PWID were referred to a local health care providers for the vaccinations.7 When antiretroviral clinical services were colocated with mobile SEP services as part of a pilot program to improve health outcomes among PWID living with HIV, CD4 lymphocyte counts, and HIV-1 RNA viral loads improved. For example, within 6 months, 85% of participants (n = 11) had viral loads less than 400 copies/mL, and by 12 months, 54% (n = 7) had continuously suppressed viral load.8 These pilot studies provide encouraging data suggesting that SEPs are an effective way to engage PWID in HIV prevention and health services that require long-term monitoring such as PrEP.
The goal of this study was to explore PrEP eligibility, willingness to use PrEP, and ability to access PrEP among PWID accessing SEP services. We frame our results within the first 3 stages of the PrEP care continuum, defined as follows: (1) confirmation of PrEP eligibility, (2) willingness to use PrEP, and (3) ability to access PrEP care.9 We focused on these stages because they are necessary precursors to the remaining stages of engagement, which include (4) receipt of a PrEP prescription, (5) initiation of PrEP, (6) adherence to PrEP, and (7) remaining engaged in care. Because previous research indicates female and male PWID have different profiles of risk10,11 and face different barriers to access health care,12–14 we stratified our analyses by sex.
METHODS
Participants
Participants were recruited from a mobile SEP in Camden County, New Jersey. From the mobile outreach van, which operates two 4-hour shifts per week, approximately 3,100 unique clients receive harm reduction services per year. These include provision of new syringes and injection drug paraphernalia (i.e., new cottons, cookers, and ties), providing rapid HIV and Hepatitis C counseling and testing, wound care, cholesterol and diabetes screening, pregnancy testing, and screening for sexually transmitted infections (STIs). Participants from this convenience sample were sequentially enrolled from July 2015 to February 2016 during the SEP's standard operating hours. Study participants included English-speaking adults 18 years and older who reported injecting illicit drugs within the past 6 months.
After providing informed consent, participants completed a technology-assisted self-interviews using a mobile tablet and self-obtained oropharyngeal, genital, and rectal specimens for chlamydia and gonorrhea screening. Participants could return for STI results 1 week later. At this follow-up visit, treatment was provided at no cost to those screening STI positive. Participants received $20 at their baseline visit and $10 when they returned for STI results. The Drexel University Institutional Review Board and the Executive Director of the agency operating the syringe exchange approved the research methods.
Survey Items
Sociodemographics . Standard survey items included age, sex, race/ethnicity, sexual orientation, housing status, educational attainment, insurance status, and income.
Drug Risk Behavior . Binary (yes/no) items were used to assess any recent (past 6 months) drug use, including heroin, cocaine, crack, methamphetamine, benzodiazepines (Xanax, Valium), marijuana, and/or club drugs (γ-hydroxybutyric acid, ecstasy, ketamine). Frequency of syringe sharing and syringe-mediated drug sharing (dividing drugs with somebody else by using a syringe; also called backloading, piggy backing, or splitting drugs wet) in the last 6 months was measured using a 5-point Likert scale (ranging from never to always ). Substance use severity was assessed with the 11-item Drug Use Disorders Identification Test (DUDIT).15 Per guidelines, DUDIT scores were calculated by summing each item (maximum score, 44).15 After summing all responses, we dichotomized the data such that scores at least 25 points are considered “high” drug dependence.
Sexual Risk Behavior . We measured vaginal and anal sex with male or female sexual partners (yes/no), total number of male and female sexual partners (continuous variable), trading sex for drugs or money (yes/no), and having a sex partner who was HIV positive (yes/no) or who injects drugs (yes/no). Condom use was measured using a 5-point Likert scale (ranging from never to always ); responses were dichotomized as “less than always” versus “always.” We also asked participants if they had been told by medical providers that they had STIs (yes/no). All of these measures focused on the last 6 months. For this study, we created a binary variable for “high” versus “low” numbers of sexual partners, defining “high” as more sex partners than the average reported by participants aged 15 to 44 years in the National Survey of Family Growth (2011–2013).16
PrEP Eligibility . PrEP eligibility was determined based on the current CDC clinical guidelines for PrEP.2 These include any affirmative response to recent injection drug use plus any one of the following: self-reported STI, sex with a person living with HIV, sex exchange, inconsistent condom use, higher than the sample mean number of sex partners reported by a national sample of men and women in the United States (by sex), syringe sharing, and drug treatment all within the previous 6 months. To these criteria, we added an STI diagnosed by the study team.17
Factors Associated With Willingness to Take PrEP . Before answering questions about PrEP, participants read a brief script adapted from the Centers for Disease Control's “PrEP Information Sheet.”18 Participants then completed 8 items, developed by Eisingerich et al.,19 assessing factors associated with willingness to take PrEP. These included 8 items measured on a 5-point Likert scale: how embarrassing participants would feel taking PrEP (very to not at all), how anxious the thought of taking PrEP would make them feel (very to not at all), willingness to tell sexual partner(s) that they are taking PrEP (definitely to definitely not), interest in taking PrEP despite potential side effects (definitely to definitely not), willingness to take PrEP if it cost $20 a month (definitely to definitely not), willingness to take PrEP even if they needed to use condoms as well (definitely to definitely not), and interest in taking PrEP if they needed to be regularly tested for HIV. Willingness to use PrEP was assessed using the question, “Given the choice of taking PrEP or not taking it at all, what would you go for?” (would take PrEP or would not take PrEP).
Health Care Utilization . Participants were asked about receiving medical care in the previous 6 months (yes/no). These included receiving care at an emergency department, medical doctor at provider's office, care at mobile outreach site, sexually transmitted disease clinic, women's reproductive health care, outpatient substance abuse services, opioid agonist treatment, or inpatient detox. Accessing opioid agonist treatment such as methadone/buprenorphine/suboxone within 6 months was assessed as a binary variable (yes/no). Finally, participants were asked about their preferences for future screening for gonorrhea/chlamydia (self-collection or collected by clinician) and venue for screening (SEP van or clinic).
Analysis
Descriptive statistics (median values and associated interquartile ranges [IQRs]) were calculated for all study variables. Nonparametric tests, including Mann-Whitney U tests for continuous data, and Pearson χ 2 or Fisher exact tests for categorical variables, were used to detect differences in distributions for men versus women. Syringe sharing and syringe-mediated drug sharing (r = 0.81, P < 0.001) were combined into one “high-risk injection drug use” variable, indicating if the respondent had either shared or engaged in syringe-mediated drug sharing in the past 6 months.
RESULTS
Study Population
The study population, described in Table 1 , included 138 PWID, 47.1% of which were women. Most of our sample (78.8%) self-identified as heterosexual, followed by 17.5% who identified as bisexual and 3.6% as gay. Participant median age was 32 years (IQR 28, 41 years). Most reported white non-Hispanic race/ethnicity (73.2%), were homeless (75%), had an income below the 2015 federal poverty guidelines of less than <$9,999 (73.2%), and were considered to have heavy drug dependence (88.4%). In our sample, the mean (SD) DUDIT score was 34.8 (8.43). Participant demographic characteristics approximated those of the clientele served by the SEP. Among approximately 3100 unique clients, 64% were male, 70% were white, and 65% were 31 years or older (M. Chavis, e-mail communication, April 2016).
TABLE 1: Individual Characteristics and Recent Drug Use Among PWID Recruited From a SEP in the Mid-Atlantic United States (N = 138)
Factors Associated With PrEP Eligibility
Nearly all (89.9%) participants were considered PrEP eligible using current CDC guidelines, and women were statistically more likely to be eligible than men (95.4% vs. 84.5%; P < 0.04; Table 2 ). Women were statistically more likely than men to report vaginal sex (81.5% vs. 56.2%; P < 0.01), exchanging sex for drugs or money (58.1% vs. 14.5%; P < 0.01), or having sex with someone living with HIV or with unknown HIV status (21.9% vs. 9.9%; P < 0.05). Women's median number of sex partners was significantly higher than men's (5 vs. 2; P < 0.04). Women were also nearly 3-fold more likely to screen positive for an STI than men (23.3% vs. 8.2%; P < 0.01). A greater proportion of men reported sex with another PWID, and similar proportions of women and men reported inconsistent condom use, STI within the preceding 6 months, and syringe sharing within 6 months. These differences were not significantly different. Receiving an opioid substitute within 6 months was relatively uncommon (21.5% among women and 12.3% among men) and not significantly different between women and men (P = 0.15).
TABLE 2: Factors Associated With PrEP Eligibility, Willingness to Use PrEP, and Ability to Access PrEP Among PWID (N = 138) Recruited From a Mobile SEP in the Mid-Atlantic United States
Willingness to Use PrEP
More than three quarters (79.3%) of participants expressed willingness to take PrEP. Women were more likely than men to express willingness (88.9% vs. 71.0%; P < 0.02). Despite these high levels of willingness, participants reported that they would feel anxious (51.6%) or embarrassed (45.0%) about taking PrEP, and half (51.4%) indicated that they would not want their sexual partner(s) to know they were taking PrEP. These feelings/attitudes did not vary significantly by sex. Most participants also indicated that they would be willing to take PrEP even if they experienced mild adverse effects (68.8%) or were required to undergo quarterly HIV screening as part of PrEP care (88.7%). However, women were more likely than men to reporting willingness to tolerate adverse effects (80.5% vs. 60.0%; P < 0.03) and quarterly HIV testing (95.9% vs. 82.5%; P < 0.03).
Ability to Access PrEP Care
As shown in Table 2 , although 67.1% were insured, few had used health services for HIV risk assessment that could lead to discussion about PrEP (at primary care physicians [43.8%], STI clinics [9.4%], or annual women's wellness examinations [15.4%]). Most participants (86%) reported that they would prefer to access future screening at the SEP versus traditional STI clinics. There were no significant differences by sex concerning insurance coverage, receiving medical care, or preference for future STI screening.
DISCUSSION
Our findings indicate that SEPs may be a viable access point to identify PWID who are be eligible for PrEP. In this sample, nearly all of those recruited were considered eligible for PrEP. Women, who represented almost half of the sample, were more likely than men to be eligible. Although both men and women reported high-risk sexual behavior, 1 in 4 women screened positive for STI (compared with 1 in 10 men). These findings are consistent with others that indicate women who inject drugs often report more HIV risk behavior10,20 and have greater HIV burden20,21 compared with their male counterparts. Given recent studies indicating that STI may be a biomarker for imminent HIV acquisition in high-prevalence networks,23,24 it seems that PWID would benefit from greater access to STI testing and treatment and PrEP services within SEPs.
In addition to sexual risk, 45% of participants reported high-risk injection drug behavior despite being recruited from a SEP where they presumably come to access harm reduction supplies including new syringes and works. Persistent injection drug risk among subsets of SEP users has been reported in other studies and may be attributable to binging on drugs (defined as injecting drugs more frequently than usual), syringe coverage (i.e., PWID face difficulty accessing as many unused syringes as they need), and drug-sharing norms.25,26 Together, these data suggest that no single intervention strategy is likely to eliminate HIV from PWID. However, it is possible that PrEP, in combination with existing effective interventions such as SEPs, could reduce HIV acquisition among those with persistent sexual and drug risk.
Our data indicate that PWID find PrEP acceptable. Despite acceptability, we noted several possible barriers to accessing PrEP, such as lack of health insurance, limited access to health care services where they would learn about PrEP, and experiencing severe substance disorders. However, SEPs are uniquely positioned to promote and provide PrEP. Syringe exchange program staff successfully engage clients for a host of services including some that require longer-term engagement in care.
Our findings should be interpreted in the context of an exploratory study with a convenience sample. Our sample size was somewhat limited, and the most of our sample identified as heterosexual. Thus, our findings may have limited generalizability to lesbian, gay, bisexual, and transgender injection drug users. In addition, we recruited PWID who access the SEP as primary exchange clients. Although this population represents a group whose HIV prevention needs are underserved, additional attention should be paid to secondary exchange clients who receive harm reduction supplies from injection drug users in their social or sexual networks. Research has shown primary and secondary SEP clients (those who do not directly access SEPs but receive clean syringes/works from peers who attend exchanges) have different risk profiles, with the secondary clients being more vulnerable.27 Recruitment of both groups in future research is critical for developing PrEP interventions that can benefit all PWID. Most importantly, we did not ask specifically about attitudes toward accessing PrEP at the SEP. Participants were recruited into a feasibility study of pairing STI control and SEP services, and nearly all reported that they would prefer to access STI services at the SEP compared with other clinical providers including an STI clinic. Therefore, research is needed to assess whether colocation of PrEP within SEPs is a feasible mechanism; however, our data and experience indicate that this concept may be acceptable to PWID.
CONCLUSIONS
Despite representing only 3% of the US population, PWID represented 6% of new HIV infections in 2015.3 If incidence rates continue unchecked, 1 in 23 women and 1 in 36 men who inject drugs will acquire HIV in their lifetime.28 Suboptimal implementation and scale-up of effective prevention interventions likely contributes to persistent or accelerating HIV epidemics in this group.6,29 Preexposure prophylaxis is an effective and underused biomedical tool in our HIV prevention arsenal. Evidence from this study and others suggests that PWID find PrEP acceptable but may face barriers to accessing it. Pairing PrEP counseling with SEP services may be one way to reduce these barriers. More research is needed to explore the acceptability and feasibility of offering and receiving PrEP services at a SEP.
REFERENCES
1. Choopanya K, Martin M, Suntharasamai P, et al. Antiretroviral prophylaxis for HIV infection in injecting drug users in Bangkok, Thailand (the Bangkok Tenofovir Study): A randomised, double-blind, placebo-controlled phase 3 trial. Lancet 2013; 381:2083–2090.
2. US Public Health Service. Preexposure Prophylaxis for the Prevention of HIV Infection in the United States—2014. A Clinical Practice Guideline [Internet]. Atlanta, GA: Centers for Disease Control and Prevention; 2014. Available at:
www.cdc/hiv/guidelines/index.html . Accessed March 10, 2017.
3. HIV in the United States: At A Glance [Internet]. Atlanta, GA: Centers for Disease Control and Prevention; 2015. Available at:
http://www.cdc.gov/hiv/statistics/overview/ataglance.html . Accessed May 1, 2016.
4. Stein M, Thurmond P, Bailey G. Willingness to use HIV pre-exposure prophylaxis among opiate users. AIDS Behav 2014; 18:1694–1700.
5. Kuo PG, Magnus M, Opoku J, et al. Willingness to use pre-exposure prophylaxis among community-recruited injection drug users. Conference on Retroviruses and Opportunistic Infections—CROI 2014; 2014; March 3–6; Boston, MA.
6. Escudero DJ, Kerr T, Wood E, et al. Acceptability of HIV pre-exposure prophylaxis (PrEP) among people who inject drugs (PWID) in a Canadian setting. AIDS Behav 2015; 19:752–757.
7. Des Jarlais DC, Fisher DG, Newman JC, et al. Providing hepatitis B vaccination to injection drug users: referral to health clinics vs on-site vaccination at a syringe exchange program. Am J Public Health 2001; 91:1791–1792.
8. Altice FL, Springer S, Buitrago M, et al. Pilot study to enhance HIV care using needle exchange–based health services for out-of-treatment injecting drug users. J Urban Health 2003; 80:416–427.
9. Liu CG, Cohen S, Bacon O, et al. The spectrum of engagement in HIV prevention: proposal for a PrEP cascade. Miami, FL: Oral abstract presented at: 7th International Conference on HIV Treatment and Prevention Adherence, 2012.
10. Evans JL, Hahn JA, Page-Shafer K, et al. Gender differences in sexual and injection risk behavior among active young injection drug users in San Francisco (the UFO Study). J Urban Health 2003; 80:137–146.
11. Bogart LM, Kral AH, Scott A, et al. Sexual risk among injection drug users recruited from syringe exchange programs in California. Sex Transm Dis 2005; 32:27–34.
12. Crystal S, Sambamoorthi U, Merzel C. The diffusion of innovation in AIDS treatment: Zidovudine use in two New Jersey cohorts. Health Serv Res 1995; 30:593–614.
13. Smith SR, Kirking DM. Access and Use of medications in HIV disease. Health Serv Res 1999; 34:123–144.
14. Copeland VC. African Americans: Disparities in health care access and utilization. Health Soc Work 2005; 30:265–270.
15. Berman A, Bergman H, Palmstierna T, et al. DUDIT: The Drug Use Disorders Identification Test Manual. Stockholm (Sweden): Karolinska Institutet, Department of Clinical Neuroscience, 2003.
16. Centers for Disease Control and Prevention. Key Statistics From the National Survey of Family Growth (2011–2013) 2015. Available at:
https://www.cdc.gov/nchs/nsfg/key_statistics/n.htm#number12months . Accessed March 14, 2017.
17. Mosher WD, Chandra A, Jones J. Sexual behavior and selected health measures: Men and women 15–44 years of age, United States, 2002. Advance data from vital and health statistics; no 362. Hyattsville, MD: National Center for Health Statistics. 2005.
18. Centers for Disease Control and Prevention. PrEP Information Sheet: Pre-exposure Prophylaxis (PrEP) for HIV Prevention 2015.
https://www.cdc.gov/hiv/pdf/prep_gl_patient_factsheet_prep_english.pdf . Accessed March 3, 2017.
19. Eisingerich AB, Wheelock A, Gomez GB, et al. Attitudes and acceptance of oral and parenteral HIV preexposure prophylaxis among potential user groups: A multinational study. PLoS One 2012; 7:e28238.
20. Bennett G, Velleman RD, Barter G, et al. Gender differences in sharing injecting equipment by drug users in England. AIDS Care 2000; 12:77–87.
21. Spittal PM, Craib KJ, Wood E, et al. Risk factors for elevated HIV incidence rates among female injection drug users in Vancouver. CMAJ 2002; 166:894–899.
22. Des Jarlais DC, Feelemyer JP, Modi SN, et al. Are females who inject drugs at higher risk for HIV infection than males who inject drugs: An international systematic review of high seroprevalence areas. Drug Alcohol Depend 2012; 124:95–107.
23. Van Der Pol B, Kwok C, Pierre-Louis B, et al. Trichomonas vaginalis infection and human immunodeficiency virus acquisition in African women. J Infect Dis 2008; 197:548–554.
24. Pathela P, Braunstein SL, Blank S, et al. The high risk of an HIV diagnosis following a diagnosis of syphilis: A population-level analysis of New York City men. Clin Infect Dis 2015; 61:281–287.
25. Wood E, Tyndall MW, Spittal PM, et al. Factors associated with persistent high-risk syringe sharing in the presence of an established needle exchange programme. AIDS 2002; 16:941–943.
26. Strathdee SA, Patrick DM, Currie SL, et al. Needle exchange is not enough: Lessons from the Vancouver injecting drug use study. AIDS 1997; 11:F59–F65.
27. Murphy S, Kelley MS, Lune H. The health benefits of secondary syringe exchange. J Drug Issues 2004; 34:245–268.
28. HIV and Injection Drug Use 2016 [Internet]. Atlanta, GA: Centers for Disease Control and Prevention; 2016. Available at:
https://www.cdc.gov/hiv/pdf/risk/cdc-hiv-idu-fact-sheet.pdf . Accessed June 29, 2017.
29. World Health Organization, UNODC, UNAIDS. Technical guide for countries to set targets for universal access to HIV prevention, treatment and care for injecting drug users, 2012 revision. Geneva: WHO, 2012.