PUBLIC HEALTH MATTERS
Greater Risk for HIV Infection of Black Men Who Have Sex With Men: A Critical Literature Review
| Gregorio A. Millett, MPH, John L. Peterson, PhD, Richard J. Wolitski, PhD, and Ron Stall, PhD, MPH
MSM. Some of the hypotheses have been pro- HIV rates are disproportionately higher for Black men who have sex with men posed or suggested by others.11–13 Our pres- (MSM) than for other MSM. We reviewed the literature to examine 12 hypotheses that might explain this disparity. entation of a hypothesis is not an implicit en- We found that high rates of HIV infection for Black MSM were partly attributa- dorsement of its premise; some hypotheses ble to a high prevalence of sexually transmitted diseases that facilitate HIV trans- are based on stereotypes or misinformed be- mission and to undetected or late diagnosis of HIV infection; they were not at- liefs about the lives of Black MSM. We criti- tributable to a higher frequency of risky sexual behavior, nongay identity, or sexual cally examined, evaluated, and summarized nondisclosure, or to reported use of alcohol or illicit substances. Evidence was the contribution of each hypothesis to ele- insufficient to evaluate the remaining hypotheses. vated infection rates among Black MSM. Future studies must address these hypotheses to provide additional explana- tions for the greater prevalence of HIV infection among Black MSM. (Am J Public METHODS Health. 2006;96:1007–1019. doi:10.2105/AJPH.2005.066720)
We searched 5 online databases: MEDLINE, HIV prevalence and incidence rates are signifi- adjustment for demographic and HIV risk PsycINFO, ERIC, AIDSLINE, and SocioFile. cantly higher for Black men who have sex with behavior covariates. Likewise, a 1998 study We considered articles published between men (MSM) than for other racial/ethnic groups found that HIV prevalence was higher among January1974 and November 2005 from of MSM in the United States.1–7 Even after the Black MSM than other MSM, and multivari- each of the databases except AIDSLINE, introduction of highly active antiretroviral ther- ate adjustment for factors that predicted HIV where only articles published between 1980 apy, the rates of disease progression and AIDS infection in the whole MSM sample did not and 2000 are available. We conducted the mortality for HIV-seropositive Black MSM ex- account for factors associated with HIV infec- literature search in 5 stages. First, we se- ceed rates for HIV-seropositive MSM of other tion in Black MSM.10 lected articles about Black populations, using races and ethnicities.8 Unexplained high HIV prevalence and in- the search terms “Black,” “African American,” Explanations of differences in HIV rates cidence rates for Black MSM continue to be and “Afro American.” Second, we conducted for MSM of different races may involve more reported 17 years after the first published re- a separate search for all articles that men- than behavior alone. Results from a 1987 port in the scientific literature. An article tioned sexual identity or behavior applicable prospective study of HIV infection among published in 2004 reported that HIV infec- to MSM, using the search terms “homosex- 1034 MSM reported higher HIV prevalence tion in young MSM was associated with older ual,” “bisexual,” “men who have sex with and incidence rates for Black MSM than for age, unemployment, being out of school, men,” “MSM,” “gay,” “same gender loving,” White MSM despite comparable reported risk having anal sex with men (irrespective of and “SGL”. Third, we cross-referenced the behaviors.9 The authors found that known condom use), and using crack cocaine during sexual identity/behavior articles with the ar- risk factors for HIV infection (i.e., multiple sex. Although young Black MSM in the sam- ticles on Black populations. Fourth, we nar- sexual partners, frequency of receptive anal ple were 9 times more likely than young rowed the citations to quantitative studies intercourse, needle sharing) did not explain White MSM to be HIV positive, the identi- conducted in the United States. Fifth, we per- the differences in HIV seroprevalence or se- fied correlates did not account for the dispro- formed a separate search across the data- roconversion between Black MSM and portionately high seroprevalence rates among bases for keywords applicable to each hy- White MSM in the sample. A similar observa- Black MSM.11 pothesis. Results from these separate searches tion was reported in 1993 by another group We performed a comprehensive review of were cross-referenced with the Black MSM of researchers who found higher rates of HIV the scientific literature reporting evidence for citations to create the universe of papers used infection for Black and Latino MSM than for and against the possible causes of higher rates for this review. We identified a total of 59 arti- White MSM.5 Multivariate adjustment for de- of HIV infection for Black MSM than for cles and 4 conference abstracts. mographic factors and risk behaviors enabled MSM of other races/ethnicities. Using data We arranged the 12 hypotheses into 3 the authors to statistically account for the from diverse samples of MSM, we collected groups: those not supported by scientific evi- high HIV prevalence rates for Latino MSM, evidence on 12 hypotheses—behavioral, psy- dence, those supported by scientific evidence, but HIV seropositivity remained indepen- chological, structural, and biological—about and those for which there was insufficient or dently associated with Black race even after the greater HIV prevalence among Black contrary evidence. A hypothesis was placed
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in the latter category when there was a lack HIV-positive MSM.17 However, Linn et al. decade, failed to support the hypothesis that of evidence for or against the hypothesis that found that reported rates of recent unpro- Black MSM engage in more sexual risk taking was specific to Black MSM (e.g., a single study tected anal sex were higher for Latino and than other MSM. or no studies) or when there were studies that Black MSM than for White MSM.30 Similarly, provided data on Black MSM but the prepon- Peterson and his colleagues found that among Hypothesis 2: Black MSM Are Less Likely derance of the evidence neither confirmed 250 Black MSM in the San Francisco Bay Than Other MSM to Identify as Gay or to nor disconfirmed the hypothesis. Scientific area, 52% reported recently engaging in Disclose Their Sexual Identity, Which May evidence was aggregated across studies to de- UAI,31 a proportion that was higher than that Lead to Increased HIV Risk Behavior termine the categorization of a given hypothe- found for White MSM in San Francisco dur- Gay identity and acculturation into the gay ses. Studies were supportive of a hypothesis ing the same time period.32 community have been associated with lower when findings were significant (P≤.05) in the Fifteen studies published since 1992 HIV-related risk behavior.42,43 If Black MSM direction of the hypothesis. Studies were non- either found no significant differences in were less likely than other MSM to identify supportive of a hypothesis when no statistical UAI for MSM of different racial or ethnic as gay, Black MSM might be more prone to difference was reported or the findings were groups6,10,16,18,19,23–25,27,28 or found that Black HIV-related risk behavior. To evaluate this significant (P≤.05) in the opposite direction MSM were less likely than other MSM to hypothesis, we reviewed studies that com- from the hypothesis. We emphasized results engage in high-risk sexual practices.11, 2 0 , 21,26,29 pared MSM by race in 4 areas: (1) sexual from multivariate analyses, but we included In contrast, only 3 studies published since identity, (2) disclosure of sexual identity or results from bivariate analyses when multi- 19 92 have reported that Black MSM engaged homosexual behavior, (3) associations be- variate data were unavailable. in higher rates of UAI with male sexual part- tween sexual identity and HIV risk behavior, ners than White MSM.33–35 A separate study and (4) associations between sexuality disclo- HYPOTHESES NOT SUPPORTED BY found that Black MSM were more likely than sure and HIV risk behavior. THE SCIENTIFIC EVIDENCE White MSM to engage in unprotected sex,36 Sexual identity. Data from several studies but the study did not differentiate between overwhelmingly supported the assertion that Hypothesis 1: Black MSM Are More vaginal and anal sex so we did not include it Black MSM are less likely than White MSM Likely Than Other MSM to Engage in in our review. to identify as gay.7,16,28,34,37,44–47 Moreover, High-Risk Sexual Behavior Number of male sexual partners. Studies studies have found that Black MSM are less Unprotected anal intercourse (UAI) and of MSM have consistently reported that com- likely than other MSM to join gay-related multiple sexual partners are longstanding pared with other MSM, Black MSM have the organizations48,49 and read gay-related sexual risk factors associated with HIV infec- same number or a smaller number of male media.28 Only 1 study found comparable tion.14 We evaluated evidence supporting and sexual partners.9,11,18,22,29,33,34,37 Aside from 3 rates of gay identification among a racially not supporting this hypothesis for each of studies of MSM that found no differences by diverse sample of MSM40; none of the stud- these risk factors. race in the reported number of male sexual ies reported higher rates of gay identification Unprotected anal intercourse. UAI is the partners,9,22,33 most studies have found that for Black MSM than for MSM of other races single most important risk factor for HIV Black MSM in comparison with White MSM or ethnicities. transmission among MSM.15 If Black MSM report fewer male sexual partners in their Disclosure of sexual identity or homosexual were more likely than other MSM to engage lifetime,11,18 fewer current male sexual part- behavior. Black MSM are less likely than in UAI, this would provide the most direct ners,18 , 2 9 , 34,37 and fewer casual male sexual other MSM to disclose their sexual identity or explanation for racial disparities in HIV infec- partners.11,18,22,29 behavior to close or casual associates. Black tion rates. However, most studies published MSM who engage in commercial sex have gay men,49 Black bisexual men,28,48 and from the first decade of the epidemic through agreater opportunity to engage in sex with young Black MSM (ages 15–29)50 are all less the present have found comparable, if not more male sexual partners than MSM who likely than their counterparts of other races lower, self-reported rates of UAI for Black do not participate in sex trade activities. In to disclose their same-sex behavior or identity MSM relative to other MSM.6,9–11,16–29 addition, commercial sex has been associated to others. One study found that as education Of 5 studies published in the first decade with HIV infection among MSM in interna- increased, White MSM were more likely and of the epidemic, 3 found no differences in tional settings.38,39 Greater commercial sex Black MSM were substantially less likely to rates of UAI practiced by MSM of different activity among Black MSM could partially disclose their sexuality.49 Investigators have racial or ethnic groups. Data from more than explain disparate HIV rates; yet, except for 1 also reported that HIV-positive Black MSM 4000 White and Black MSM in 5 cities col- study,28 most domestic comparative studies are less likely17 , 51 than other HIV-positive lected before the first cases of AIDS were of MSM by race have reported no racial dif- MSM or are equally likely52 to disclose their reported (1978–1979) showed comparable ferences in the prevalence of commercial sex sexual orientation to members of their sup- rates of UAI for the 2 groups.22 These re- work activity.11,33,40,41 port network. sults were replicated by a seroprevalence To summarize, most studies we reviewed, Sexual identity and HIV risk behavior. study of MSM9 and by a small pilot study of particularly those conducted in the past Few studies of MSM have examined sexual
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identity as a predictor for HIV risk behav- Hypothesis 3: Black MSM Are More alcohol use,33 alcohol-related problems,61,63 or ior by race or ethnicity. The few that have Likely Than Other MSM to Abuse alcohol use during sex.16 In addition, in ran- stratified by race when reporting sexual Substances, Especially Injection Drugs, dom samples of young MSM, Black MSM identity have failed to report HIV risk be- That Increase Their Risk for HIV have reported comparable64 or lower20,59 havior by race and sexual identity.28,45,46 Infection rates of alcohol consumption and lower rates However, 2 studies that recruited only Injection drug use and sexual activity while of substance dependence 59 than other MSM. Black MSM tested the association between under the influence of substances have been Studies of injection drug use by Black sexual identity and HIV risk. Hart and associated with HIV risk behavior.55–57 If MSM have had somewhat mixed results. In- Peterson found that among 758 young Black MSM were more likely than other jection drug use was found to be greater Black MSM of varying sexual identities, MSM to use mind-altering substances, it among Black MSM than among White MSM sexual identity did not predict participation could partially explain observed racial differ- in 2 studies.36,60 However, 5 other studies in receptive or insertive UAI.53 Another ences in HIV prevalence. However, pub- found that Black MSM were equally as likely study of 174 Black MSM reported that gay- lished studies relevant to this hypothesis re- as or less likely than other MSM to report in- identified Black MSM were more likely vealed a complex picture. jection drug use.5,11,20,29,40 Similarly, Black than non–gay-identified Black MSM to en- Young Black MSM are as likely as or less MSM were equally as likely as5 or less likely gage in sexual risk taking behavior.54 likely than other MSM to report drug use. than9,11 other MSM to report needle sharing. Disclosure of sexuality and HIV risk behav- Studies of Black MSM aged 13 through 29 Reports of drug use during sex also varied ior. Few studies have tested for associations years report that compared with their non- among racial groups of MSM. Although between disclosure of sexual identity and Black peers, young Black MSM engage in young Black MSM (aged 15 through 22 HIV risk behavior. Most studies have exam- lower general illicit drug use20,58 and compa- years) were less likely than other young MSM ined disclosure rates by MSM in the absence rable or lower use of amphetamines, barbitu- to report drug use during sex,11 McKirnan et of behavioral risk data49,51,52 or tested inde- rates, LSD, nitrites, tranquilizers, and pow- al.16 and Heckman et al.33 found that older pendent associations between race and dis- dered cocaine.11, 5 9 Contrasting results were Black MSM were more likely than their non- closure and race and HIV risk behav- found only for marijuana and heroin use. Black peers to use drugs during sex. ior.17 ,18 , 2 8 These limitations were not found One study found comparable59 and another Black MSM are significantly more likely in 3 studies of disclosure. A 1992 study study found greater20 use of marijuana and than other MSM to report using noninjected found that Black MSM who were uncomfort- heroin among young Black MSM relative to crack cocaine. Sullivan and colleagues re- able disclosing their sexuality to others were other young MSM. ported that Black MSM were 3 times as likely more likely than Black MSM who were “out” Studies of older cohorts of MSM have also as White MSM to report crack cocaine use.60 to engage in unsafe sex.31 In contrast, a found comparable or lower drug use among In a multiracial sample of MSM, 94% of all 2002 study found that Black MSM who Black MSM than among other MSM.36,60–62 crack cocaine users were Black.16 A third scored lower on a scale that included mea- Siegel et al. found no differences in use of study found that more Black MSM than sures of sexuality disclosure reported taking hard drugs (i.e., crack, cocaine, heroin, White MSM used cocaine during sex,33 but fewer sexual risks than Black MSM who speed) among a diverse sample of MSM the authors did not differentiate between scored higher on the scale.54 Similarly, aged 50 years or older.36 Likewise, among crack cocaine and powdered cocaine. No- among 1100 young Black MSM, men who another racially diverse sample of MSM, tably, there may be differences in crack co- did not disclose their sexual orientation to Irwin and Morgenstern found no differences caine use between younger and older others were less likely than those who did in the reported use of opiates, cocaine, hallu- Black MSM. Two studies using probability disclose to have 5 or more male sexual part- cinogens, or other drugs (i.e., ketamine, Ec- samples of young MSM found that young ners during their lifetime, to report having stasy, γ-hydroxybutyrate).61 A separate study Black MSM were as likely as59 or significantly UAI with male sexual partners, and to have of 10000 HIV-positive MSM reported that less likely than11 other young MSM to report an HIV-positive test result.50 Black MSM were significantly less likely than having ever used crack cocaine. To summarize, Black MSM are less likely non-Black MSM to use diazepam, hallucino- To summarize, Black MSM are no more than other MSM to identify themselves as gens, or nitrites.60 In addition, the same likely than other MSM to report drug or alco- gay or to disclose their homosexual behav- study and 2 other studies61,62 found a lower hol use. Crack cocaine is the only illicit drug ior to others. However, having a nongay prevalence of amphetamine use among that Black MSM report using more often identity does not increase HIV risk-taking Black MSM than among MSM of other than other MSM. It is not known whether behavior with male sexual partners among races/ethnicities. high rates of crack cocaine use for Black MSM. In contrast, recently published Black MSM are just as likely as or less Black MSM make a significant contribution studies of Black MSM have found that sexu- likely than other MSM to consume alcohol. to racial differences in HIV prevalence. Also, ality nondisclosure was associated with Except for 1 investigation,61 studies have it is unclear whether Black MSM are more lower sexual risk taking with male sexual found no differences among MSM of different likely than other MSM to combine substance partners. races and ethnicities in the prevalence of use and sex.
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HYPOTHESES SUPPORTED BY THE comparable STD prevalence rates5,29,77,78 less likely to be aware of their HIV-positive SCIENTIFIC EVIDENCE across all racial/ethnic groups, and none of status than are other MSM. Men who are un- the studies we reviewed reported a lower aware of their HIV infection are more likely Hypothesis 4: Black MSM Are More prevalence of STDs among Black MSM than to engage in behaviors that may transmit the Likely Than Other MSM to Contract among other MSM. virus to HIV-negative partners than are men Sexually Transmitted Diseases That To summarize, there is evidence that Black who know their positive status.83 Infrequent Facilitate the Acquisition and MSM are more likely than other MSM to re- or delayed HIV testing contributes to the Transmission of HIV port having an STD, which contributes to the high HIV prevalence among Black MSM. Sexually transmitted diseases (STDs) in- observed racial differences in HIV disease crease vulnerability to65 and transmissibility burden. HYPOTHESES FOR WHICH THERE IS of 66 HIV infection. Recent STD outbreaks INSUFFICIENT OR CONFLICTING have heralded increasing rates of high-risk Hypothesis 5: Black MSM Are Less SCIENTIFIC EVIDENCE sex among MSM in the United States.67–71 Likely Than Other MSM to Be Tested One of the notable aspects of the outbreaks for HIV or to Know Their HIV Status, Hypothesis 6: Black MSM Are Genetically among American MSM has been the high and They May Unknowingly Expose More Susceptible to HIV Than Other MSM rate of HIV coinfection among men with a Their Sexual Partners to HIV Individuals differ in their susceptibility to recent diagnosis of syphilis or gonorrhea.72 Compared with other MSM, Black MSM HIV infection. Some remain uninfected de- Although the reported outbreaks have prima- are equally likely7,28,33,80 or more likely79 to spite repeated exposure to HIV, and others rily involved HIV-positive White MSM, racial have ever been tested for HIV. One study become infected after a single exposure.84 comparative studies have documented greater found no racial differences among persons Several genetic and biological characteristics STD coinfection in HIV-positive Black MSM tested for HIV among 4000 MSM tested be- that affect susceptibility to HIV infection than in other HIV-positive MSM.5,7 Among tween 1990 and 1999 in New York City.7 have been identified.85,86 If these character- several thousand MSM in New York City who Similar results were reported in 3 other stud- istics were differentially distributed between were tested for HIV, Torian et al. found that ies,28,33,80 and an additional study found that racial or ethnic groups, they might con- HIV-positive Black MSM were significantly Black MSM were significantly more likely tribute to differences in HIV incidence and more likely to be coinfected with gonorrhea, than White MSM to report a history of HIV prevalence rates for Black and other MSM. syphilis, or nongonococcal urethritis than testing.79 However, there is evidence that Of the potential genetic factors that may af- HIV-positive White MSM (60% vs 18%).7 Black MSM are tested less frequently and fect risk for HIV infection, CCR5 receptors, Similarly, Easterbrook et al. reported that later in their HIV infection than other MSM. which are used by HIV to infect cells, have HIV-positive Black MSM were significantly A recent multisite seroprevalence study re- received the most attention. Persons who are more likely than HIV-positive White MSM to ported that young Black MSM (aged 15–22 homozygous for the CCR5 base 32 protein have syphilis, but there were no differences in years) were tested for HIV less frequently deletion do not express CCR5 receptors and urethral gonorrhea among seropositive MSM than young White MSM.81 In addition, signifi- are relatively rare in the general population in their sample.5 cantly more HIV-positive young Black MSM (< 1%).87 Studies have confirmed that per- STD rates are also higher for Black MSM than HIV-positive young Latino or White sons who are homozygous or heterozygous than for other MSM regardless of HIV sero- MSM were unaware of their HIV infection for the genetic mutation may be resistant to status. Black MSM are more likely than other (91%, 69%, and 60%, respectively).25,81 Simi- HIV infection.85–93 Among HIV-positive per- MSM to report ever having had an STD or lar results were found in another sample of sons, the genetic mutation has also been as- currently having an STD.20,33,73 These find- young MSM.29 However, high rates of unrec- sociated with decreased viral load, less rapid ings are supported by recent STD surveillance ognized HIV infection are not limited to progression of HIV disease, and increased data from the Centers for Disease Control young Black MSM. In a multisite investigation survival.94–96 and Prevention (CDC), which found that that recruited older cohorts of MSM (aged Approximately 1% of Whites globally are Black MSM were more likely than other 18–81 years), 64% of Black MSM, 18% of homozygous for the genetic variant, and 15% MSM to report urethral chlamydia infection, Latino MSM, and 11% of White MSM were are heterozygous (i.e., 1 CCR5 base 32 allele urethral gonorrhea, and pharyngeal gonor- unaware of their HIV infection.80 Moreover, and fewer CCR5 receptors).87 Fewer persons rhea.74 Studies have also found that propor- a separate study reported that a significantly of African or Asian descent are homozygous tionally more Black MSM than White MSM greater proportion of HIV-positive Black (< 0.1%) or heterozygous (< 1%) for the receive a diagnosis of or report a history of MSM were tested later in their HIV infection CCR5 base 32 allele.97–99 The few studies hepatitis B.5,16,75,76 Although the presence of (within 2 months to a year of AIDS diagnosis) that have examined the CCR5 mutation hepatitis B itself does not contribute to HIV than were their White peers.82 among MSM have failed to recruit sufficient risk, infection with hepatitis B is a marker of To summarize, Black MSM are just as likely samples of Black MSM to report stratified HIV risk-related behaviors (e.g., unprotected as other MSM to receive an HIV antibody analyses by race.88–90,93 One study of MSM sex or injection drug use). Four studies found test, but they are tested less frequently and are pointedly restricted analyses to White
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participants because of the documented low rates of HIV infection among Black MSM. However, racial differences among MSM prevalence of CCR5 base 32 deletion in non- Latino men in general are less likely to be who accessed and used health care have been White populations.90 circumcised than Black men.10 9 ,110 Assuming reported. HIV-positive Black MSM were sig- To summarize, there is insufficient infor- that Latino MSM are also less likely to be cir- nificantly more likely than other MSM to re- mation on the degree to which genetic fac- cumcised than Black MSM, HIV infection ceive care at public clinics112 and less likely to tors affect HIV prevalence among Black rates for Latino MSM should be higher than discuss HIV-related concerns with a doctor or MSM. The fact that CCR5 base 32 deletion rates for Black MSM. But proportionally more nurse.52 In addition, although 1 study found occurs less frequently in populations of Black MSM than Latino MSM in the United no differences in outpatient visits among color97 gives some credence to a genetic States have been diagnosed with HIV infec- MSM of different races,114 another study component for racial differences in HIV in- tion since the beginning of the epidemic (cu- found racial differences in outpatient use ac- fection among MSM. However, Asian popu- mulatively, 30% vs 12%, respectively, and cording to CD4 count.113 White MSM with lations are just as unlikely as Black popula- 27% vs 18%, respectively, in 2003 alone).1 CD4 counts higher than 500 cells per cubic tions to express the genetic mutation,97 but To summarize, there are insufficient data to millimeter were 10 times as likely as Black rates of HIV infection for Asian MSM in the evaluate the role that circumcision plays in MSM with comparable CD4 counts to report United States remain significantly lower than HIV infection among Black MSM. Studies an outpatient visit during the past 6 those for Black MSM.1 have found that White MSM are more likely months.113 No differences in use of outpatient than non-White MSM to be circumcised and services were found among HIV-positive Hypothesis 7: Black MSM Are Less Likely that circumcised MSM are less likely than un- MSM with more compromised immune sys- Than Other MSM to Be Circumcised, circumcised MSM to be HIV-positive, but tems (<500 cells per cubic millimeter), re- Increasing Their Risk for HIV Infection there are no data specific to Black MSM. gardless of race. Circumcision is a cultural practice with bio- ART access and adherence. ART decreases logical consequences that may protect a man Hypothesis 8: HIV-Positive Black MSM viral load and infectiousness in HIV-positive from HIV infection.100,101 Studies have found Are Infectious for a Longer Time Than persons.115 If HIV-positive Black MSM were that in the United States, Black men are less Other HIV-Positive MSM less likely than other HIV-positive MSM to likely than White men to be circumcised. Black HIV-positive MSM may be infectious have access to ART, it might explain the high Cook et al. reported that 76% of White men for a longer period of time than other HIV- HIV transmission rates among Black MSM. in a sample drawn from an urban STD clinic positive MSM, contributing to greater oppor- In 3 studies, Black MSM reported less ac- were circumcised, compared with 18% of tunities for HIV transmission. Factors that in- cess to ART than other MSM.112 ,116 ,117 Jacob- Black men.10 2 Another study of nearly 8000 fluence the duration of infectiousness among son et al. reported that HIV-positive Black male patients at a US military clinic found HIV-positive Black MSM are (1) access to MSM were less likely than HIV-positive men that 85% of Whites and 34% of Blacks were and use of medical care for HIV infection of other racial/ethnic groups to be taking circumcised.10 3 Likewise, in a sample of 1410 and (2) access and adherence to antiretro- ART.116 Halkitis and colleagues found less men, Laumann et al. found that Black men in viral therapy (ART). ART access among Black MSM at 1 of 2 proj- 2 of 3 age cohorts born between 1933 and HIV-related medical care access and use. ect sites.112 Likewise, Stall et al. found that a 1973 were significantly less likely to be cir- High viral load has been associated with a comparison group of Black and Latino MSM cumcised than were White men.10 4 CDC data greater likelihood of transmitting HIV to sex- were less likely than White MSM to receive indicate that circumcision rates among new- ual partners.111 Inadequate health care access recommended levels of ART.117 However, a born boys were 10% higher for Whites than or suboptimal health care use by HIV-posi- fourth study reported no differences in ART for Blacks between 1979 and 1993 but that tive Black MSM may result in their having access among 307 HIV-positive MSM accord- White and Black rates converged in the late higher viral loads and, in turn, an increased ing to race/ethnicity.113 1990s.10 5 likelihood of transmitting HIV to their sexual Viral load and HIV transmissibility are Three studies have evaluated the role of partners. Several quantitative studies have also influenced by adherence to ART regi- circumcision in HIV infection in MSM.10 6–108 explored health care access and use by mens.118 Differences in ART adherence One small study found no association be- racially diverse samples of HIV-positive among HIV-positive MSM of different races tween circumcision and HIV infection10 6 ; 2 MSM. They found that HIV-positive Black and ethnicities could partially explain the studies found a protective effect associated MSM were as likely as HIV-positive White disproportionately high rates of HIV infec- with circumcision.10 7 ,10 8 None of the 3 studies MSM to report having health insurance,112 ,113 tion among Black MSM. However, only 2 stratified analyses by Black race, but 1 of the including private health insurance.113 In addi- investigations of ART adherence that we re- studies reported that non-White MSM collec- tion, they found no differences among HIV- viewed stratified MSM by race, and the 2 tively were less likely than White MSM to be positive MSM of different racial/ethnic studies differed in their results.112 ,119 ,12 0 In a circumcised.10 7 groups in terms of emergency department longitudinal study of 539 HIV-positive The protective effect of circumcision alone visits,113 ,114 inpatient visits,113 or recent MSM, Kleeberger and colleagues found that cannot explain the disproportionately high hospitalizations.114 Black race was an independent predictor of
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119 TABLE 1—Summary of Findings for Hypotheses Addressing Disproportionate HIV Prevalence nonadherence to ART at baseline and 12 0 and Incidence Among Black Men Who Have Sex With Men (MSM) at 2-year follow-up. However, no differ- ences in ART adherence were found in a Supportive Studies Nonsupportive Studies racially diverse sample of 463 HIV-positive Hypotheses not supported by the scientific evidence MSM recruited from San Francisco and New 112 1. Black MSM are more likely than other MSM to engage in York City. high-risk sexual behavior. To summarize, the data for this hypothesis 35,a 26,a are mixed. Despite comparable health insur- Black MSM have higher rates of unprotected anal Bingman et al., 2001 Bartholow et al., 2005 ance coverage among HIV-positive MSM, intercourse than other MSM. Gomez and Halkitis, 199834 Bingham et al., 200329,a HIV-positive Black MSM either do not have Heckman et al., 199933 Denning et al., 200527 adequate access to preventive health care or Linn et al., 198930 Doll et al., 199022 use preventive health care services less opti- Peterson et al., 199231 Harawa et al., 200411,a mally than other HIV-positive MSM. More- Lemp et al., 19946,a over, HIV-positive Black MSM are less likely MacKellar et al., 200525,a than other HIV-positive MSM to report access Mansergh et al., 200219 to ART. However, the available data on ART McKirnan et al., 200116 adherence among MSM of different races are McKirnan et al, 199528 inconclusive. Ostrow et al., 199117 21,a Peterson et al., 2001 Hypothesis 9: Black MSM Are More 23 Purcell et al., 2005 Likely Than Other MSM to Have Sex 10 Ruiz et al., 1998 With Partners Known to Be HIV Positive 9 Samuel and Winkelstein, 1987 A greater likelihood of having an HIV- 24 Solorio et al., 2003 positive sexual partner might explain the dis- 18 Stokes et al., 1996 parate rates of HIV prevalence. Three 20,a Valleroy et al., 2002 racially diverse studies of MSM have exam- Black MSM have a larger number of male sexual partners . . . Bingham et al., 200329,a ined reports of sex with HIV-positive part- than other MSM. Doll et al., 199022 ners, but the data are mixed. In 1 study, Gomez and Halkitis, 199834 Black MSM were more likely than White Harawa et al., 200411,a MSM to know or suspect that a recent male Heckman et al., 199933 sexual partner was HIV-positive.33 In 2 other Kramer et al., 198037 studies, Black MSM were significantly less Samuel and Winkelstein, 19879 likely than other MSM to report having had 5,11 Stokes et al., 199618 sex with a man who was HIV positive. Black MSM are more likely than other MSM to engage in McKirnan et al., 199528 Harawa et al., 200411,a One of the 2 studies found no association commercial sex work. Heckman et al., 199933 among Black MSM between HIV-positive Newman et al., 200441 status and reported sex with an HIV-positive 5 Rietmeijer et al., 199840 partner. The authors of the second study 2. Black MSM are less likely than other MSM to identify as concluded that even if Black MSM had re- gay or to disclose their sexual identity, which may lead ported high rates of sex with partners to increased HIV risk behavior. known to be HIV positive, this still would Black MSM are less likely than other MSM to be Chu et al., 199244 Rietmeijer et al., 199840 not have accounted for the disparate rates 11 gay-identified. Doll et al., 199245 of HIV infection. To summarize, the contribution of this hy- Goldbaum et al., 199846,a pothesis to HIV infection rates among Gomez and Halkitis, 199834 Black MSM is not known. Data from the 3 Kramer et al., 198037 studies relevant to this hypothesis were lim- McKirnan et al., 199528 ited because the studies required that partici- McKirnan et al., 200116 pants know the HIV status of their sexual Montgomery et al., 200347 partners, but infected male sexual partners of Torian et al., 20027 study participants could have been unaware Continued of or reluctant to disclose their HIV-positive status.
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TABLE 1—Continued Hypothesis 10: The Sexual Networks of Black MSM Place Them at Greater Risk Black MSM are less likely than other MSM to disclose Kennamer et al., 200049 Mason et al., 199752,b for HIV Infection Than the Sexual their sexuality to others. Mason et al., 199752,a,b Networks of Other MSM McKirnan et al., 199528 Sex between members of different popula- CDC, 200350,a tions (sexual mixing) facilitates the spread of 17 Ostrow et al., 1991 sexually transmitted disease.121–123 Research 51,a Simoni et al., 1997 has found that young MSM whose male sex- 48 Stokes et al., 1996 ual partners are older are more likely to be 54 Nongay identity among Black MSM is associated with . . . Crawford et al., 2002 HIV-positive than young MSM whose male 53,a high-risk sex. Hart and Peterson, 2004 sexual partners are closer to their own age.12 4 31 54 Nondisclosure of sexuality among Black MSM is Peterson et al., 1992 Crawford et al., 2002 Several studies have suggested, but not em- 50,a associated with high-risk sex. CDC, 2003 pirically determined, that the sexual networks 3. Black MSM are more likely than other MSM to abuse of Black MSM increase their likelihood of substances, especially injection drugs, that increase HIV infection5,10,11,125 Only 1 published study their risk for HIV infection. tested the effect of sexual mixing on HIV in- 62 Black MSM are more likely than other MSM to use drugs. . . . Halkitis et al., 2005 fection among Black MSM. Data from more 11,a Harawa et al., 2004 than 400 young MSM (aged 23–29 years) 61,a Irwin et al., 2005 indicated that proportionally more Black 59,a McNall et al., 1999 MSM were HIV positive than were MSM of 36 Siegel et al., 2004 any other racial/ethnic group.29 The authors 60 Sullivan et al., 1998 also found that racial differences in partner 58 Torian et al., 2002 selection partially explained elevated rates of 20,a Valleroy et al., 2002 HIV infection for Black MSM. Black MSM 61,a,c 64,a Black MSM are more likely than other MSM to use or Irwin et al., 2005 Greenwood et al., 2002 were more likely than other MSM to report 33 abuse alcohol. Heckman et al., 1999 having anal sex with Black male sexual part- 61,a,c Irwin et al., 2005 ners, and they were significantly more likely 16 McKirnan et al., 2001 than White MSM to report having anal sex 59,a McNall et al, 1999 with a male partner of a different age group 63,a Stall et al., 2001 (younger or older). More important, the rela- 20,a Valleroy et al., 2002 tive odds of HIV infection among Black MSM 36 29,a Black MSM are more likely than other MSM to use Siegel et al., 2004 Bingham et al., 2003 decreased by 20% after the authors adjusted 60 5 injection drugs. Sullivan et al., 1998 Easterbrook et al., 1993 for older sexual partners and anal sex with Harawa et al., 200411,a Black partners in multivariate analyses. Rietmeijer et al., 1998 40 To summarize, the data provided by the Valleroy et al., 200220,a single available study are strong, and their Black MSM are more likely than other MSM to use drugs McKirnan et al., 200116 Harawa et al., 200411,a value is limited only by the lack of additional during sex. Heckman et al, 199933 studies with which to properly evaluate this Black MSM are more likely than other MSM to use Heckman et al., 199933,d Harawa et al., 200411,a hypothesis. Regardless of whether Black crack cocaine. McKirnan et al., 200116 McNall et al, 199959,a MSM know their partners’ HIV status, the Sullivan et al., 199860 sexual networks and sexual mixing patterns Hypotheses supported by the scientific evidence of Black MSM likely contribute to the dispro- 4. Black MSM are more likely than other MSM to contract CDC, 200274 Easterbrook et al., 19935,e portionately high rates of HIV infection sexually transmitted diseases that facilitate the Easterbrook et al., 19935,e Bingham et al., 200329,a among these men. acquisition and transmission of HIV. Heckman et al., 199933 Geisler et al., 200277 Landrum et al., 198873 Kim et al., 200378 Hypothesis 11: Black MSM Are More MacKellar et al., 200175,a,f Likely Than Other MSM to Be McKirnan et al., 200116 Incarcerated, Which Increases the Ostrow et al., 199976 Likelihood of Exposure to HIV Torian et al., 20027 It has been widely speculated that high Valleroy et al., 200220,a HIV infection rates among Black MSM are Continued partly because of high incarceration rates for Black men and subsequent homosexual
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12 6–128 TABLE 1—Continued contact while in prison. Adequate cir- cumstantial evidence supports these specula- 5. Black MSM are less likely than other MSM to be tested tions. Black men represent the largest propor- for HIV or know their HIV status, and may unknowingly tion of all incarcerated men in federal and expose their sex partners to HIV. state prisons12 9 and the largest proportion of Black MSM are less likely than other MSM to have been . . . Dao et al., 1999 79 HIV-infected men in jails and state and fed- tested for HIV. Heckman et al., 199933 eral prisons.13 0 In addition, homosexual con- McKirnan et al., 199528 tact131 and STD and HIV132–135 outbreaks CDC, 200580,a have been documented among men in protec- Torian et al., 20027 tive custody settings, the HIV infection rate is Black MSM are tested for HIV less frequently than CDC, 200281,a ... 5 times higher in prisons than in the general other MSM. population,13 6 and fewer than 1% of correc- Black MSM are more likely than other MSM to have Bingham et al., 200329,a ... tional facilities nationally permit the distribu- unrecognized HIV infection. MacKellar et al., 200525,a tion of latex condoms.13 7 CDC, 200281,a Despite these data, few studies of MSM CDC, 200580,a have explored racial differences in incarcera- Black MSM are more likely than other MSM to be Wortley et al., 199582 ... tion history and HIV infection. Disparate re- diagnosed with HIV late in the disease’s progression. sults were reported in 2 studies of young Hypotheses for which there is insufficient or conflicting scientific evidence MSM. One study found no racial differences 29 6. Black MSM are genetically more susceptible to HIV than ...... in reported incarceration history, while the other MSM (Black MSM are less likely to have the other found that young Black MSM were sig- CCR5 base 32 allele) nificantly more likely than other young MSM 20 7. Black MSM are less likely than other MSM to be ...... to report a history of incarceration. Neither circumcised, increasing their risk for HIV infection. study tested for associations between incar- 8. HIV-positive Black MSM are infectious for a longer time ceration history and HIV status. However, a than other HIV-positive MSM. third study tested the association between HIV-positive Black MSM are less likely than other MSM . . . Halkitis et al., 2003112 incarceration and HIV status among Black to have health insurance. Kass et al., 1999113 men in Los Angeles, Calif. Among men who HIV-positive Black MSM are less likely than other MSM Kass et al., 1999113,g Kass et al., 1999113,g had been incarcerated, 23% of case subjects to have access to health services. Zucconi et al., 1994114 and 9% of control subjects reported having HIV-positive Black MSM are less likely than other MSM Mason et al., 199752 ... had anal sex while in jail, prison, or a deten- 13 8 to discuss HIV-related concerns with their health tion center. When the researchers con- care providers. trolled for anal sex while not incarcerated, HIV-positive Black MSM are less likely than other MSM Halkitis et al., 2003112 Kass et al., 1999113 men who reported having anal sex during to be receiving antiretroviral therapy. Jacobson et al., 2001116 incarceration were not at greater risk for Stall et al., 2001117,a HIV infection. In fact, the men reported hav- HIV-positive Black MSM are less likely than other MSM Kleeberger et al., 2001119 Halkitis et al., 2003112 ing had significantly more anal intercourse 120 with male sexual partners outside rather to adhere to antiretroviral therapy medication regimens. Kleeberger et al., 2004 than inside penal institutions (45% vs 16%, 9. Black MSM are more likely than other MSM to have sex Heckman et al., 199933 Easterbrook et al., 19935 respectively). However, the men also re- with partners known to be HIV positive. Harawa et al., 200411,a ported greater condom use during anal sex 10.The sexual networks of Black MSM place them at greater Bingham et al., 200329,a ... outside rather than inside penal institutions risk for HIV infection than the sexual networks of (90% vs 42%, respectively), and a greater other MSM. proportion of case subjects than control sub- 11. Black MSM are more likely than other MSM to be jects reported that they were always the re- incarcerated, which increases the likelihood of ceptive partner during anal sex while incar- exposure to HIV. cerated (43% vs 18%). Black MSM are more likely than other MSM to have a Valleroy et al., 200220,a Bingham et al., 200329,a To summarize, Black MSM are more likely history of incarceration. than other MSM to report a history of incar- Black MSM have higher rates of participation in anal sex . . . Wohl et al., 2000138 ceration. However, the single study to date while incarcerated than outside correctional facilities. that tested the association between imprison- Continued ment and HIV infection among Black MSM found no association. There is a dearth of
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TABLE 1—Continued to report having had an STD in the past or to have a current diagnosis of STD. The Black MSM are more likely to use condoms during anal Wohl et al., 2000138 ... presence of an STD makes Black MSM more sex outside rather than inside correctional facilities. susceptible than other MSM to acquisition HIV infection is associated with a history of incarceration . . . Wohl et al., 2000138 and transmission of HIV. Second, Black among Black MSM. MSM are less likely than other MSM to 12. Black MSM are more likely than other MSM to engage Easterbrook et al., 19935 ... know their HIV status and to be tested for in anorectal douching, which increases their risk for HIV early in the progression of their disease. HIV infection. Likewise, rates of unrecognized HIV infec- tion are greater among Black MSM than Note. CDC=Centers for Disease Control and Prevention.A study was supportive of a hypothesis when findings were significant (P≤.05) in the direction of the hypothesis; a study was nonsupportive of a hypothesis when no statistical difference was other groups of MSM. reported or the findings were significant (P≤.05) in the opposite direction from the hypothesis. Three hypotheses were not supported by a Subjects were randomly recruited MSM. the available data. The studies we reviewed b Mason et al.52 found that, compared with other HIV-positive MSM, HIV-positive Black MSM were less likely to disclose their sexuality to health care providers (supportive evidence) but as likely to disclose their sexuality to parents and lovers showed that, contrary to popular belief, (nonsupportive evidence). Black MSM do not engage in more HIV risk c 61 Irwin et al. found that Black MSM reported consuming a significantly higher number of drinks per day than other MSM behavior than other MSM, and that, among (supportive evidence), but they found no differences among MSM of various races in problem drinking (nonsupportive evidence). d Authors did not distinguish between crack cocaine and powdered cocaine. Black MSM, HIV risk behavior is not associ- e Easterbrook et al.5 found that HIV-positive Black MSM were significantly more likely than HIV-positive White MSM to have ated with nongay identity but may be in- syphilis (supportive evidence), but they found no differences in urethral gonorrhea among HIV-positive MSM in their sample versely related to nondisclosure of sexual (nonsupportive evidence). f In MacKellar et al.,75 Asian MSM had the highest prevalence of hepatitis B infection, followed by Black MSM.White MSM had identity. In addition, the preponderance of the lowest prevalence of hepatitis B infection. evidence to date has not shown that Black g 113 Kass et al. found that, compared with other HIV-positive MSM, HIV-positive Black MSM were less likely to use outpatient MSM engage in greater rates of substance services (supportive evidence) but equally likely to have private health insurance, to have made emergency visits, to have made inpatient visits, and to have had recent hospitalizations (nonsupportive evidence). use than other MSM. The available studies neither supported nor refuted 7 hypotheses. However, it should not be assumed that these factors fail studies that would allow us to properly evalu- MSM who engaged in anorectal douching to contribute to differences in HIV infection 14 6 ate this hypothesis. were 5 times as likely to be HIV positive ; rates between Black MSM and MSM of however, the authors did not stratify the other races/ethnicities. Despite the absence Hypothesis 12: Black MSM Are More analyses by race. The second study, which of data, it is unlikely that known biological Likely Than Other MSM to Engage in did stratify by race, found that Black MSM factors that prevent HIV infection (e.g., Anorectal Douching, Which Increases were significantly more likely than other CCR5 or circumcision) operate differently 5 Their Risk for HIV Infection MSM to report anorectal douching. Addi- among Black MSM than in the general pop- Although the use of nonoxynol-9 in the tionally, compared with Black MSM who did ulation of Black men, but additional re- anal cavity has been associated with the exfo- not report anorectal douching, Black MSM search is needed to gauge the extent to liation of rectal epithelial cells,13 9 ,14 0 the de- who did were significantly more likely to be which structural factors (e.g., sexual net- gree to which douching, or rinsing out the HIV positive. works, health care access, incarceration) and anal cavity with water or a water-based solu- To summarize, Black MSM are significantly behavioral factors (e.g., having sex with tion, affects anal tissue is not known.141 Scien- more likely than other MSM to report anorec- known HIV-positive partners, anorectal tific investigations have examined vaginal tal douching, and studies have found associa- douching) contribute to disproportionately douching more commonly than anal douch- tions between anorectal douching and HIV- high HIV infection rates among Black MSM. ing,14 2 and vaginal douching has been related positive status among Black MSM. However, The high background prevalence of HIV to STD acquisition.14 3 But vaginal mucosa are there are too few studies to permit evaluation and the sexual mixing patterns of different from anal mucosa.141 Some have of this hypothesis. Black MSM might make several of these suggested that the probability of HIV acquisi- factors more central to HIV transmission tion or transmission may be greater during CONCLUSIONS among Black MSM than among MSM of anal sex than during vaginal sex because rec- other races/ethnicities. tal tissue is more prone to abrasion during The results of our literature review are Future studies should resolve the discrep- penetration.14 4 ,14 5 summarized in Table 1. Partial explanations ancy between low self-reported sexual risk Only 2 studies of MSM have examined as- for the disproportionate HIV rates for Black behavior and high STD prevalence among sociations between anorectal douching and MSM, in comparison with other MSM, were Black MSM. Only 2 studies have examined HIV infection. One found that, compared supported by 2 hypotheses. First, compared social desirability bias among MSM,11, 3 0 and with MSM who did not report douching, with other MSM, Black MSM are more likely no studies of MSM have used standardized
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measures, such as the Marlowe–Crowne References transmission between male sexual partners. Am J Epi- scale,14 7 to explore differences in socially de- 1. Centers for Disease Control and Prevention. HIV/ demiol 1999;150:306–311. AIDS Surveillance Report, 2003 (Vol. 15). Atlanta, Ga: sirable responses. Future studies should also 16. McKirnan DJ, Vanable PA, Ostrow DG, Hope B. Centers for Disease Control and Prevention; 2004: Expectancies of sexual “escape” and sexual risk among investigate the role of sociocultural factors 34–35. Also available at: http://www.cdc.gov/hiv/ drug and alcohol-involved gay and bisexual men. J Subst (e.g. racial discrimination, homophobia, and stats/hasrlink.htm. Accessed April 22, 2004. Abuse. 2001;13:137–154. stigmatization) in the disparate rates of HIV 2. Valleroy LA, MacKellar DA, Karon JM, et al. HIV 17. Ostrow DG, Whitaker RED, Frasier K, et al. 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Sero- Abstracts of the XIV International AIDS Conference; July 7–12, 2002; Barcelona, Spain. Abstract The human toll experienced by Black prevalence of HIV and risk behaviors among young homosexual and bisexual men: the San Francisco/ MoPeC3429. MSM as a consequence of HIV infection war- Berkeley Young Men’s Survey. JAMA. 1994;272: 21.Peterson JL, Bakeman R, Stokes J, Community rants increased research efforts that are spe- 449–454. Intervention Trial for Youth Study Team. Racial/ethnic cifically designed to identify the underlying 7. Torian LV, Makki HA, Menzies IB, et al. HIV in- patterns of HIV sexual risk behaviors among young men who have sex with men. J Gay Lesbian Med Assoc. causes of the AIDS epidemic among Black fection in men who have sex with men, New York City Department of Health sexually transmitted disease clin- 2001;5:155–162. MSM. Our findings support the need for ef- ics, 1990–1999: a decade of serosurveillance finds 22. Doll LS, Judson FN, Ostrow DG, et al. Sexual be- fective structural interventions that reduce that racial disparities and associations between HIV havior before AIDS: the hepatitis B studies of homo- HIV risks at the community level through and gonorrhea persist. Sex Transm Dis. 2002;29: sexual and bisexual men. AIDS. 1990;4:1067–1073. 73–78. better access to and utilization of STD and 23. Purcell DW, Moss S, Remien RH, Woods WJ, 8. Blair JM, Fleming PL, Karon JM. Trends in AIDS HIV detection and treatment. Parsons JT. 2005. Illicit substance use, sexual risk, and incidence and survival among racial/ethnic minority HIV-positive gay and bisexual men: differences by se- men who have sex with men, United States, 1990– rostatus of casual partners. AIDS. 2005;19(suppl 1): 1999. J Acquir Immune Defic Syndr. 2002;31:339– S37-S47. 347. 24. Solorio R, Swendeman D, Rotheram-Borus MJ. About the Authors 9. 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HIV MPH, Centers for Disease Control and Prevention, 1600 Sex Trans Dis. 1998;25:100–107. Clifton Rd, Mail Stop E-45, Atlanta, GA 30333 (e-mail: sexual risk behavior over 36 months of follow-up in [email protected]). 11. Harawa NT, Greenland S, Bingham TA, et al. As- the world’s first HIV vaccine efficacy trial. J Acquir Im- This article was accepted July 3, 2005. sociations of race/ethnicity with HIV prevalence and mune Defic Syndr. 2005;39: 90–101. HIV-related behaviors among young men who have 27. Denning PH, Campsmith ML. Unprotected anal sex with men in 7 urban centers in the United States. intercourse among HIV-positive men who have a J Acquir Immune Defic Syndr. 2004;35:526–536. Contributors steady male sex partner with negative or unknown All authors contributed to the development of the hy- 12. Malebranche D. Black men who have sex with HIV serostatus. 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