JAIDS Journal of Acquired Immune Deficiency Syndromes:
HIV Among People Who Use Drugs: A Global Perspective of Populations at Risk
Stockman, Jamila K PhD, MPH; Strathdee, Steffanie A PhD
From the Department of Medicine, Division of Global Public Health, University of California San Diego, La Jolla, CA.
Correspondence to: Steffanie A. Strathdee, PhD, Department of Medicine, Division of Global Public Health, University of California San Diego, 9500 Gilman Drive, MC 0507, La Jolla, CA 92093-0507 (e-mail: firstname.lastname@example.org).
This article examines the epidemiology of HIV among selected subgroups of drug users around the world who are “most at risk”-men who have sex with men, female sex workers, prisoners, and mobile populations. The underlying determinants of HIV infection among these populations include stigma, physical and sexual violence, mental illness, social marginalization, and economic vulnerability. HIV interventions must reach beyond specific risk groups and individuals to address the micro-level and macro-level determinants that shape their risk environments. Public health interventions that focus on the physical, social, and health policy environments that influence HIV risk-taking in various settings are significantly more likely to impact the incidence of HIV and other blood-borne and sexually transmitted infections across larger population groups.
Illicit drug use, particularly injection drug use, accounts for significant proportions of new HIV infections in Eastern Europe, South America, and east and southeast Asia,1 where the estimated prevalence of HIV infection among some injecting drug user (IDU) subpopulations exceeds 40%.1 In this article, we focus on the epidemiology of HIV among some of the most vulnerable populations, including men who have sex with men (MSM), male-to-female (MTF) transgender persons, female sex workers (FSWs), incarcerated individuals, and mobile populations. We also highlight the role of shared contextual factors and aspects of the risk environment that contribute to the spread of HIV among these groups because their commonality may suggest opportunities for the development of new interventions.
MEN WHO HAVE SEX WITH MEN
In the United States, HIV surveillance data show MSM to be the only behavioral risk group with increasing incidence.2 Estimates of HIV incidence in MSM averages 1.55 per 100 person-years3 but is likely higher among MSM who are ethnic minorities and MSM who inject drugs (MSM-IDU).
MSM are vulnerable to HIV for many reasons, including social marginalization, stigma, sexual abuse and victimization, suicidality, and high levels of drug and alcohol use, especially among men who do not identify as gay or bisexual.4 MSM-IDUs may be doubly stigmatized and isolated because of their dual identities, experiencing homophobia by IDUs because they are MSM, and stigma from MSM because they are IDUs. The recent increase in HIV among MSM in the United States, particularly among young MSM of color, has been attributed to several factors, including safer sex fatigue and a reduced concern about HIV now that effective antiretroviral therapies are available.5 However, increases in use of methamphetamine and other “club drugs” are also critical factors. Methamphetamine is typically snorted or smoked, or injected, and more rarely, inserted rectally. Rates of methamphetamine injection vary widely by region and subgroup.6 In a sample of HIV-positive MSM methamphetamine users in San Diego, CA, 42% had ever injected drugs, and those who did so were more likely to be bisexual, report more health and social problems, and score higher on measures of impulsivity, low social support, and social rejection.7 In San Francisco, 52% of MSM at 2 HIV outpatient clinics reported injection methamphetamine use,8 and in Los Angeles County, 39% of MSM who had used methamphetamine in the lifetime reported injection drug use.9
Methamphetamine use among MSM, including gay, bisexual, nonidentifying MSM, and MTF transsexuals, is prevalent in the United States, Australia, and western Europe,3 and the incidence of HIV is 2-3 times higher among MSM who use methamphetamine/amphetamines compared with MSM who do not.3 In the United States, 13% of adult MSM residing in Chicago, Los Angeles, New York, and San Francisco reported using methamphetamine in the past 6 months.10 Among MSM aged 15-22 years surveyed in 7 US urban areas, 20% reported methamphetamine use in the prior 6 months.11 The Sydney Gay Community Period Survey in Australia found that, between 2002 and 2005, methamphetamine use in the past 6 months increased from 26% to 39% among HIV-positive MSM and from 14% to 22% among HIV-negative men.12 In London, England, researchers found that methamphetamine use among MSM ranged from 19.5% for men surveyed in gyms, 12.6% for those in HIV treatment, and 8.3% for those in HIV testing clinics.13 Methamphetamine use has been associated with increased risks for transmission of multidrug-resistant HIV.3 MSM who use methamphetamine often engage in high-risk behaviors, including unprotected sex with multiple partners, marathon sex, and polydrug use.14-17 A recent review found that methamphetamine use was causally associated with HIV infection, although the evidence was inconclusive as to whether the causal pathway was direct, indirect, or both.18
The epidemiology of HIV among MSM in the United States and other developed countries has been well characterized, whereas that among MSM in sub-Saharan Africa is only now garnering attention. In 2007, the prevalence of male same-sex behavior in the general population was estimated at 0.03%-0.9% in Kenya, 0.06%-3.6% in South Africa, and 2.3% in Tanzania.19 HIV prevalence among African MSM was estimated to range from 7.8% in Sudan to 34.3% in Cape Town,19 and the estimated incidence of HIV was 20.4 per 100 person-years among MSM in Mombasa, Kenya, most of whom were male sex workers.19
Few studies have examined potential linkages between the epidemic of HIV and the epidemic of drug abuse in Africa.20 Among drug-using MSM in Cape Town, Durban, and Pretoria, South Africa, considerable overlap was found for drug use and sexual risk behaviors, with high rates for use of crack cocaine and heroin, risky sexual behavior, and HIV transmission.20 Recent attempts to criminalize homosexuality in Uganda and Kenya are likely to drive the behavior underground but not end it and to undermine public health efforts in HIV prevention. Such policies subvert the health and human rights of sexual minorities and will only help to fuel the HIV epidemic.
Unfortunately, few of the interventions for MSM who use drugs have proven efficacious or sustainable. Interventions for nonidentifying MSM may benefit from addressing community norms, sexual identity, and stigma as underlying factors that contribute to drug use and sexual risk behaviors.21 Interventions for bisexual and nonidentifying MSM-IDUs should consider race/ethnicity and social and contextual factors, such as internalized homophobia and fear of disclosure.22 Consideration should also be given to the potential risks of HIV transmission to their male sexual partners and their female sexual partners and heterosexual IDUs.21,23,24
HIV prevention research focused on MSM-IDUs of color in the United States should consider the cumulative effects of racism, stigma, and homophobia, and contextual, structural, and socioeconomic factors, including class, income, and education.25 Higher rates of HIV incidence among black MSM despite comparable rates of drug use as other racial/ethnic groups need to be understood if the Nation's efforts to fight HIV are to succeed. Recent literature suggests that the risk network may play a role. For example, partner concurrency and assortative mixing among black MSM may limit partner selection and concentrate risks for HIV transmission within the network, especially when background HIV prevalence is high.26,27 Of course, HIV is an equal opportunity virus, transmitted by anyone who comes in contact with infected blood, whether through syringe sharing, unsafe sex, or unsafe injection behaviors with intimate partners.23
MTF TRANSGENDER POPULATIONS
MTF transgender persons are at risk for drug abuse and HIV, and many have been found to inject hormones but not to have undergone sex reassignment. Data on HIV prevalence and drug use among MTF transgender persons are sparse. In a review of 29 studies focusing on MTF transgender persons, HIV prevalence was high, but ranged widely from 16% to 68%.28 Across studies, MTF transgender persons reported comparable rates of injecting hormones (weighted mean, 27.0%) or silicone (weighted mean, 24.7%) and a much lower rate of injecting street drugs (eg, heroin, crack) (weighted mean, 12.0%). Nine studies reported low levels of sharing needles when injecting drugs (weighted mean, 2.0%) or when injecting hormones or silicone (weighted mean, 6.0%)28; however, 26.7% reported using crack or other illicit drugs.28 Extreme marginalization of many MTF transgender persons may lead to sex work, which poses other risks, including violence, HIV, and sexually transmitted infection acquisition through unprotected sex. Interventions targeting drug using MTF transgender persons should address a multiplicity of risk factors, including psychosocial and behavioral factors, and the stigma associated with gender identity and ethnicity, particularly as it relates to ethnic minority MTF transgender persons.29
FEMALE SEX WORKERS
Sex workers play a unique role in HIV and sexually transmitted infection epidemics as they are at risk of both acquiring and transmitting infections from and to their clients and noncommercial sex partners, serving as an “epidemiological bridge” between high-risk groups to the general population.30 Sex workers often report histories of sexual/physical abuse, and revictimization by intimate partners, pimps, clients, and police, which can predispose toward psychological distress, depression, anxiety, disempowerment, and substance use.31-33 Criminalization of sex work in most countries displaces street prostitution to less visible areas, increasing their vulnerability to violence and assault.34,35 The multiple vulnerabilities faced by sex worker populations, including entrenched poverty, substance abuse, repeated violence and sexual assault, stigma, and mental illness, may directly or indirectly increase their risks of HIV infection. Although female, male, and transgender sex workers all experience higher rates of HIV infection relative to the general population, most epidemiologic studies have focused on FSWs.
High levels of substance use among FSWs may be antecedents or sequela of the harsh realities of survival sex work or both. In some cases, stimulants such as cocaine and methamphetamine may be used to conserve energy or stay awake during long work hours.36 In many settings, overlap between FSW and IDU populations is considerable, making them at dual risk for infection through both the sexual and parenteral routes. Studies in some countries have found HIV prevalence among FSWs who inject drugs to range from 1.4% in Lithuania, 12.3% in Mexico, 2.0%-35.4% in Europe, 16.6%-65.0% in Russia, and 10.0%-22.4% in the United States.37
Injection and noninjection drug use are associated with HIV infection among FSWs. In Yunnan, China, lifetime injection and noninjection drug use were independently associated with HIV infection among FSWs.38 Among FSWs in the Mexico-US border cities of Tijuana and Ciudad Juarez, Mexico, injection of cocaine and snorting/smoking methamphetamine were associated with HIV infection.39 In San Francisco, sex work was the strongest predictor of HIV infection among female IDUs, who had a 5-fold elevated odds of HIV seroconversion.23
Analyses of data from 70 countries suggest that the number of HIV-infected FSWs is the strongest predictor of country-wide HIV prevalence in the general population.40 The global sex industry has been increasing41 but, as estimated by the World Health Organization, fewer than 15% of FSWs have adequate access to HIV prevention resources.42 These findings underscore the pressing need for interventions to reduce HIV incidence among FSWs and their contacts, especially in low-resource settings. Such interventions should include safer sex negotiation skills within the context of ongoing drug use, so women can protect themselves from infection by their regular partners and clients37 and link to referrals for drug treatment, HIV testing, HIV treatment, and care.43-45
Interventions are needed that reflect the heterogeneity of the FSW population in terms of culture, geographic space, social context, and sociodemographic characteristics. Interventions for those engaged in survival sex work will likely differ from those who are trafficked or controlled by pimps/managers or others.46 Sex workers who are also mothers will likely have special needs if they have dependent children at home. Interventions appropriate for commercial venues (eg, brothels, hotels, bars, massage parlors) will likely be less so in public or semipublic spaces (eg, streets, parks, cars). Sensitivity to violence, sexual assault histories, trauma, abuse, and mental illness should always be a priority because many FSWs have had or are having these types of experiences and will have special needs.47,48 Addressing such complexities although also addressing HIV requires an ethical, holistic, and nonjudgmental approach that empowers FSWs to protect themselves by using female condoms and vaginal microbicides,49,50 although also building self-esteem, promoting new skills, and facilitating alternative economic opportunities.43,51
Clients of FSWs are at risk of acquiring HIV, transmitting it to their partners, and diffusing it to the wider population. Few HIV prevention interventions have targeted FSW clients, although their knowledge of condoms and regular use of them with their commercial and other sex partners will impact their safety and the potential wider spread of disease.52-54 Similarly, few programs have focused on the intimate (nonpaying) partners of sex workers although unprotected sex is common among FSWs and their intimate partners.53,55-59 These relationships and the influences they can have on risk behaviors need further study32,60 because of their potential public health impact on HIV diffusion from unprotected sex and drug use between FSWs, their intimate partners, and/or their paying clients.
Incarceration, illicit drug use, and HIV constitute a multiplicity of risk. In the United States, this trifecta particularly afflicts African American men whose incarceration rates for drug related and other crimes far exceed those for non-blacks.61 In 2003, African Americans were 5 times more likely than whites to have been to jail, and 44% of the prisoners under federal or state jurisdiction were African Americans.62
Incarceration is a marker and a risk factor for HIV infection. It disrupts social networks and family relationships and leads to economic vulnerability, cumulative disadvantage, and limited access to educational opportunities and social and risk reduction services.63-65 HIV vulnerability among incarcerated populations, both in and out of prisons, come from multiple sources, including needle sharing among incarcerated IDUs, unsafe and unprotected sex between incarcerated men, drug use and unprotected sex upon prison release, resumption of risky and criminal activity (trading sex for money or drugs, or drug dealing) after release, and little if any use of HIV prevention and treatment services, which may be due to drug use relapse, difficulty accessing appropriate services or continued stigma associated with being an ex-convict.61,62,66-69 Exposure to contaminated tattooing equipment and forced sex may also be a risk factor for HIV infection.70-72 In most countries, there is no access to sterile syringes, condoms, or opiate substitution therapy for incarcerated populations. In countries where these services are available, reductions in HIV risk behaviors among incarcerated IDUs have been documented.73
A range in HIV prevalence among IDU prisoners has been reported in developing and transitional countries: 3.0% in Mexico, 9.9% in Brazil, 42% in China, 46% in Russia, 50% in Serbia, 56% in Indonesia, 60% in Libya, 63% in Iran, and 80% in Manipur.74 Few data exist that document the risk of acquiring HIV while under detention. However, in a serological study of 499 male IDUs incarcerated in Tehran, Iran, the prevalence of HIV at intake was 24.4% and the incidence of HIV upon release was 16.8%.75
Interventions are needed to reduce injection and syringe sharing among prisoners and to reduce risks for sexual acquisition and transmission among drug using men who have sex with other men while incarcerated.76 These are highly sensitive and complicated matters, but in many countries, there is a deep-seated reluctance to adapt evidence-based interventions for prison populations, such as needle and syringe programs, bleach and decontamination strategies, and opioid substitution therapies. The fact is that many prisoners are released back to their families and communities, which means they will bring their infections, illnesses, and diseases with them. This is why such reluctance must be overcome not only for the health of individual prisoners but also for the wider public health of their communities.
Mobile populations include migrants, refugees, deportees, temporary workers, victims of human or sex trafficking, and those displaced by war, famine, political and social upheaval, and man-made and natural disasters. Mobile populations often experience physical, social, and cultural isolation, homelessness, poverty, and a greater sense of vulnerability and anonymity, which can heighten risks for HIV and other infections.77-80 Mobility itself can increase the chance of encountering HIV-positive persons81 who bridge higher to lower risk populations that ordinarily would not interact.82 Mobility can also influence membership and change within sexual networks.83 Transportation routes, interstate highways, and borders are natural pathways for the diffusion of HIV and other diseases.84 Stressors and environmental conditions (eg, loss of traditional social environment, physical, social and/or cultural isolation, long work hours)85,86 that lead to homelessness and transiency may increase intermixing with others at risk, leading to drug use, sex trading, violence victimization, HIV, and other social ills.
Prevalence estimates of illicit drug use are difficult to obtain and vary widely among diverse migrant populations. The prevalence of injection drug use has been estimated at 2.1% among migrant FSWs in the United States Virgin Islands,87 22.0% among migrant Mexican middle school students in Texas, United States,88 and 12.6% among male and 16.6% among female migrants in Mexico.89 Crack or cocaine use was recently estimated at 16.7% among returning migrants in Mexico.90
Migration has been reported as a risk factor for HIV in China, where migrant MSM and FSWs report high rates of injection drug use and needle sharing.91,92 Numbers of temporary migrants seeking employment in China have also grown from 11 million in 1982 to 79 million in 2000.
A recent study of IDUs in Tijuana, Mexico, found that males deported from the United States had 4-fold higher odds of HIV infection.93 In contrast, female IDUs migrating to Tijuana had higher odds of HIV infection with increased time in Tijuana,93 suggesting that they acquired the infection there. HIV risks seem to vary by the types and reasons for migration, by gender and age, and by other social and economic factors. Understanding these variations can lead to improved HIV interventions for migrants, tailored to their cultural and socioeconomic contexts and communities. In border settings, a coordinated binational response will help to ensure that HIV interventions reflect shared commitments to immigration and public health policies although working to reduce barriers and engage those at risk to seek drug treatment and HIV testing and treatment services.94 Mobile clinics are an innovative approach for providing mobile, hard-to-reach, and remote populations with access to health services, including HIV testing and counseling, and condom and syringe distribution,84 and health promotion information mental health, prevention screening, and managing stressors associated with substance abuse.84
The high prevalence of HIV among drug using populations is a substantial source of morbidity and mortality around the world and results from shared risk factors and environmental conditions, typically characterized by physical and sexual violence, mental illness, poverty, stigma, neglect, isolation, and discrimination, that is, underlying determinants that are exogenous to the individual.95,96 HIV interventions must reach beyond specific risk groups and individuals to address the micro-level and macro-level determinants that shape their risk environments. Public health interventions that focus on the physical, social, and health policy environments that influence HIV risk-taking in various settings are significantly more likely to impact the incidence of HIV and other blood-borne and sexually transmitted infections across larger population groups, especially in low-resource settings.97,98
This work was supported by National Institutes of Health grants R25 DA025571 and T32 DA023356 from the National Institute on Drug Abuse. The authors also thank Thomas Patterson and Irene Iuppa for their assistance. The contents of this article are solely the responsibility of the authors and do not necessarily represent the official views of the National Institutes of Health or National Institute on Drug Abuse.
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female sex workers; HIV; injection drug use; men who have sex with men; mobile populations; prisoners
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