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Sex Differences in Risk Factors for HIV Seroconversion Among Injection Drug Users
A 10-Year Perspective
Steffanie A. Strathdee, PhD;
Noya Galai, PhD;
Mahboobeh Safaiean, MPH;
David D. Celentano, ScD;
David Vlahov, PhD;
Lisette Johnson, MA;
Kenrad E. Nelson, MD
Arch Intern Med. 2001;161:1281-1288.
ABSTRACT
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Background Injection drug use directly or indirectly accounts for nearly half the
annual human immunodeficiency virus (HIV) infections in the United States.
Prospective studies that investigate both sexual and parenteral HIV risks
among injection drug users (IDUs) are needed. We studied factors for HIV seroconversion
among male and female IDUs in Baltimore, Md.
Methods The HIV-negative IDUs (1447 male and 427 female) were recruited into
a prospective study from 1988 to 1989 or in 1994. Participants underwent semiannual
HIV tests and surveys through December 1998. Poisson regression was used to
identify risk factors for HIV seroconversion, stratified by sex. Behaviors
were treated as time-dependent covariates that varied at each semiannual period.
Results Subjects were primarily African American (91%), and median age at enrollment
was 35 years. Incidence of HIV was 3.14 per 100 person years (95% confidence
interval, 2.78-3.53) and did not significantly differ by sex. Younger age
independently predicted HIV seroconversion for both men and women. Among men,
factors that independently predicted HIV seroconversion were the following:
less than a high school education, recent needle sharing with multiple partners,
daily injection, and shooting-gallery attendance. The incidence of HIV was
double for men recently engaging in homosexual activity and cocaine injection.
Among women, the incidence of HIV was more than double for those recently
reporting sexually transmitted diseases.
Conclusions The incidence of HIV remained high among IDUs in Baltimore over the
past decade. Risk factors for HIV seroconversion differed markedly by sex.
Predominant risks among men included needle sharing and homosexual activity;
among women, factors consistent with high-risk heterosexual activity were
more significant than drug-related risks. Human immunodeficiency virus interventions
aimed at IDUs should be sex-specific and incorporate sexual risks.
INTRODUCTION
SINCE THE human immunodeficiency virus (HIV)/acquired immunodeficiency
syndrome (AIDS) epidemic began in the early 1980s, the proportion of HIV/AIDS
cases attributed to men having sex with men has significantly declined, with
subsequent increases among heterosexuals and injection drug users (IDUs).1-3 Taking into account
direct transmission of HIV infection through sharing contaminated injection
equipment and indirect transmission to sexual partners and offspring, injection
drug use accounts for nearly half the annual total number of HIV cases in
the United States.3
The changing dynamic of the HIV/AIDS epidemic has had a significant
impact on women and minorities. Women accounted for 23% of all reported adult
AIDS cases in the United States in 1999,1 which
represents a doubling over the past decade. Injection drug use accounts for
42% of all reported AIDS cases among women and adolescent girls.1
The proportion of HIV/AIDS cases diagnosed among African Americans and Hispanics
has significantly increased.1-2
These ethnic groups accounted for 55% of the cumulative total number of AIDS
cases and 77% of AIDS cases in women and girls reported through December 1999.1
Rates of IDU-associated AIDS cases have been consistently higher in
the northeastern region of the United States, where a large population of
IDUs (primarily heroin injectors who began injecting in the 1960s) already
existed prior to the HIV epidemic.4-5
Compared with the United States overall, injection drug use accounts for a
significantly higher proportion of AIDS cases in Maryland (54% vs 36%, respectively,
in 1999).1, 6 In Baltimore, Md,
the prevalence of HIV infection in a community-based cohort of IDUs at enrollment
in 1988 was 24%,7 which has given rise to persistently
elevated HIV incidence rates.
Because early studies of IDUs suggested that most HIV infections were
due to needle sharing,8-9 it has
generally been assumed that sexual transmission was negligible or was overshadowed
by parenteral routes.10-12
Although some studies suggested an important role for heterosexual transmission,13-15 few published reports
have prospectively examined both drug-related and sexual risk factors for
HIV seroconversion among male and female IDUs.
We examined both drug-related and sexual risk factors for HIV transmission
in a cohort of more than 1800 IDUs for a 10-year period. A large study sample
and extended follow-up enabled us to study potential sex differences in HIV
risk factors, taking into account changing behaviors over time. Such data
are critical for developing appropriate interventions to reduce HIV incidence
among marginalized IDU populations, including women and ethnic minorities.
METHODS
STUDY POPULATION
From 1988 to 1989, a total of 2946 persons who were at least 18 years
old were recruited into a longitudinal study of the natural history of HIV
infection in IDUs in Baltimore. Potential participants were recruited through
extensive community outreach, as described elsewhere.7, 16
All participants were free of an AIDS-defining illness at enrollment and had
a history of illicit injection drug use within the previous 10 years. After
providing informed consent (approved by the Committee on Human Research, Johns
Hopkins School of Hygiene and Public Health, Baltimore), participants underwent
interviewer-administered questionnaires, physical examinations, and blood
specimen collection.
Of 2946 subjects at enrollment, 708 (24%) were HIV-seropositive and
2238 (76%) were seronegative. Of the HIV-negative subjects, 1560 (70%) returned
for at least 1 follow-up visit, at which time they were invited to enroll
in a study of risk factors for HIV infection. A detailed analysis comparing
participants who returned with those who did not has been reported.17 To replenish cohort numbers because of losses to
follow-up, HIV seroconversion (n = 218), and deaths (n = 261), 363 HIV-seronegative
current IDUs were additionally recruited in 1994, 338 (93%) of whom returned
for at least 1 follow-up visit.
To be eligible for analysis, participants were required to be HIV-seronegative
at enrollment and to have returned for at least 1 follow-up visit. Human immunodeficiency
virus seroconverters for whom there was more than a 3-year interval between
their last HIV-negative and first HIV-positive test were also excluded (24
of 301 seroconverters). Therefore, a total of 1874 persons were included in
the present analysis.
Semiannual interviews collected data on drug use history, sociodemographics,
and drug use and sexual behavior within the last 6 months. At each study visit,
HIV seroconverters were identified by commercial HIV antibody enzyme-linked
immunosorbent assay. Repeatedly, seropositive specimens were confirmed by
Western blot. All participants received their HIV test results, including
pretest and posttest HIV counseling, administered by trained interviewers.
STATISTICAL ANALYSIS
Incidence density of HIV infection was calculated using person-time
methods, taking into account varying lengths of follow-up between December
1988 and December 1998. The date of seroconversion was considered to be the
midpoint between the last seronegative and first documented seropositive HIV
test result. Incidence rates were examined by exposure variables of interest
(eg, sex and age). All behavioral data were obtained through self-reported
survey data with the exception of data pertaining to needle exchange program
(NEP) attendance, which was obtained from the Baltimore NEP using a reverse
identifier based on portions of select information (eg, last 4 digits of the
participant's social security number).
Poisson regression was used to calculate relative incidence for exposure
variables per semiannual period, stratified by sex. The mean was proportional
to semiannual periods and the antilog of the linear combination of covariates,
whose weights represented the regression coefficients.18
Behavioral data and variables reflecting use of specific services within the
last 6 months (eg, attendance at NEP and methadone maintenance programs) were
treated as time-dependent covariates that were subsequently updated for each
semiannual period. Since the Baltimore NEP was introduced in August 1994,
variables pertaining to NEP attendance were coded as 0 for all study visits
prior to this date. For each exposure variable, potential sex differences
were examined by assessing interaction terms. In cases of missing data, values
for the preceding semiannual visit were assumed reliable for a maximum of
1 year, after which time values were treated as missing.
To determine the independent effect of covariates of interest on the
outcome of HIV seroconversion, multivariate Poisson models were generated.
To take into account temporal trends in HIV seroconversion, we adjusted for
calendar year. Goodness of fit was assessed by assessing the deviance of a
model from the saturated model, based on differences in degrees of freedom.
Statistical significance was determined by comparing nested models using the
likelihood ratio test. The relative contribution of each exposure variable,
adjusting for the simultaneous effects of all covariates in the final models,
was expressed in terms of adjusted relative incidence rates (ie, rate ratios).
RESULTS
Of 1874 eligible participants, 1447 (77%) were male and 427 (23%) were
female. Most subjects (91%) were African American. The median age and duration
of injection drug use at enrollment were 35 years (interquartile range [IQR],
30-40 years) and 14 years (IQR, 6-24 years), respectively. In comparing cohort
members who returned for at least 1 visit from 1988 to 1989 with subjects
additionally recruited in 1994 there were significant differences in age at
enrollment (34.7 vs 37.1 years; P < .001) and
in the proportions who were male (80.3% vs 63.0%; P
< .001) and African American (89.78% vs 95.27%; P
= .002).
In the 6 months prior to enrollment, 91% of our subjects reported having
injected drugs. Of a total of 17 021 study visits, the median number
of visits was 7.8 per person (IQR, 3-12); the median interval between study
visits was 6.5 months (IQR, 5.5-6.9 months). Among a total of 8826.45 person
years (PYs) of observation, 277 documented HIV seroconversions occurred for
a global HIV incidence rate of 3.14 per 100 PYs (95% confidence interval [CI],
2.78-3.53). Human immunodeficiency virus incidence declined significantly
over time from 4.58 per 100 PYs in 1988 to 1.29 per 100 PYs in 1998; this
translated to a 10% decrease per year (rate ratio, 0.90 per year). Despite
our earlier finding that female IDUs had significantly higher HIV incidence
compared with male IDUs,17 during the extended
10-year follow-up period HIV incidence remained only slightly higher among
women (3.23 per 100 PYs) compared with men (3.11 per 100 PYs). The rate ratio
for HIV seroconversion among women vs men was 1.04 (95% CI, 0.8-1.4).
Sex-specific HIV incidence rates associated with specific demographic
and behavioral characteristics are summarized in Table 1. Higher rates of HIV seroconversion occurred among both
men and women aged 30 years or younger at enrollment. In addition, significantly
higher HIV incidence rates occurred among those who injected cocaine alone
or in combination with other drugs, injected daily or more, shared injection
paraphernalia (eg, cotton, cookers, and water), had multiple needle-sharing
partners, and had a sexually transmitted disease (STD). Among men, annual
prevalence rates for gonorrhea and syphilis varied between 0.52% and 4.63%
and 0.30% and 1.72%, respectively; for female IDUs these rates were generally
higher, varying annually from 1.47% and 7.14% and 0.61% and 4.50%, respectively.
Human immunodeficiency virus incidence for persons who injected cocaine alone
was 7.20 per 100 PYs among women and 5.05 per 100 PYs among men.
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Table 1. Risk Factors Associated With HIV Seroconversion Among Male
and Female IDUs (1988-1998)*
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To assess whether HIV incidence and specific risk factors differed for
male and female IDUs, Poisson regression models were constructed, stratifying
by sex (Table 2). Among men, higher
annual income and higher levels of education were inversely associated with
HIV seroconversion, but this was not the case for women. Homelessness, number
of needle sharing partners, and shooting-gallery attendance (locations where
IDUs gather to buy or rent syringes and/or inject drugs in groups) were associated
with an increased risk of HIV seroconversion, but only among men. Recent enrollment
in a methadone maintenance program was inversely associated with HIV seroconversion
for women (rate ratio, 0.40; 95% CI, 0.19-0.84). Among women, HIV incidence
was elevated for those who reported using coccaine; a similar association
was not observed for men.
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Table 2. Rate Ratios for Specific Exposures Associated With HIV Seroconversion
Among Male and Female IDUs*
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Sex differences were more striking in terms of sexual risks (Table 2). Men who reported recently engaging
in homosexual activity were 4 times more likely to become infected with HIV
(rate ratio, 4.04; 95% CI, 1.5-10.9). Among female IDUs, HIV incidence was
more than double among those who reported recently having sex with another
IDU (rate ratio, 2.27; 95% CI, 1.3-3.8). Among women, condom use was significantly
associated with an increased risk of HIV seroconversion, which is not surprising
because condom use is highly correlated with high-risk sexual behaviors (eg,
sex trade). Rate ratios for male IDUs compared with women differed significantly
for reporting sex with an injection drug–using partner, numbers of heterosexual
partners, and homosexual activity.
After simultaneously taking into account multiple risk factors for HIV
infection that were permitted to vary over time, younger age was the only
risk factor that remained independently associated with the risk of HIV seroconversion
for both men and women (Table 3). Injection drug users who were younger than 30 years at enrollment were more
than twice as likely to experience HIV seroconversion. Among men, independent
predictors of HIV seroconversion included sociodemographic, drug-related,
and sexual risks. Having achieved at least a high school education was inversely
associated with HIV seroconversion, whereas injecting daily or more, injecting
cocaine, and attending shooting galleries were associated with an increased
risk of HIV transmission. Male IDUs recently engaging in homosexual activity
were more than twice as likely to seroconvert compared with those who reported
no recent homosexual contact, whereas men reporting 1 or more heterosexual
partners were almost half as likely to seroconvert compared with those reporting
no recent heterosexual partners.
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Table 3. Independent Risk Factors for HIV Seroconversion Among Male
and Female IDUs (1988-1998)*
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Among female IDUs, none of the drug-related variables associated with
HIV incidence in univariate models retained statistical significance after
taking into account other risk factors. After adjusting for the effects of
age and time, female IDUs having a recent STD increased the risk of HIV seroconversion
more than 2-fold (rate ratio, 2.52; 95% CI, 1.39-4.58).
Since our study sample comprised subjects who were recruited from 1988
to 1989 and in 1994, we repeated the above analyses, restricting to the former
sample. Independent predictors of HIV seroconversion were identical and the
magnitude of observed associations did not appreciably differ.
COMMENT
The major findings of this study were 2-fold: first, after accounting
for parenteral risks related to HIV seroconversion among IDUs, sexual risks
played a significant role, and second, HIV risk factors among IDUs differed
markedly by sex. Whereas drug-related risk behaviors and homosexual activity
were the most important predictors of HIV seroconversion among men, factors
consistent with high-risk heterosexual activities were the main predictors
among women. Because this study was based on longitudinal data from more than
1800 IDUs for a 10-year period, we were able to uncover associations that
may not have been observed by others because of low statistical power or lack
of a prospective design. Our results offer new directions for HIV prevention
among highly marginalized injection drug–using populations that remain
at high risk for infection.
The only common predictor of HIV seroconversion that we observed among
male and female IDUs was younger age. Injection drug users aged 30 years or
younger at enrollment were more than twice as likely to seroconvert compared
with those aged 40 years or older. This is consistent with several reports
that indicate that younger IDUs are more likely to engage in needle-sharing
and other behaviors that place them at higher risk of acquiring HIV and hepatitis
B or C viruses.14, 16, 19-23
Compared with older drug users, younger IDUs tend to have initiated injection
more recently; specific factors related to initiation into injection (eg,
number of "trainers" who teach new initiates how to inject) may be associated
with elevated HIV transmission risks.23 Young
drug users should be a focus for intensive interventions aimed at preventing
substance abuse and reducing the spread of blood-borne pathogens.
Not unexpectedly, we observed a high risk of HIV infection associated
with injection-related behaviors that are associated with needle-sharing behaviors
(eg, cocaine injection and shooting-gallery attendance), which is consistent
with early reports.8-9 Injection-related
risks were more pronounced among men, in whom cocaine injection and shooting-gallery
attendance were independent risk factors for HIV seroconversion. The finding
that cocaine injection is strongly associated with HIV seroconversion supports
several previous studies.9-11
Compared with heroin injectors, cocaine injectors lead more chaotic lives,
inject and share needles more frequently, and are more likely to engage in
the sex trade, elevating their risk of HIV infection.
Shooting galleries were identified as strong correlates of HIV infection
earlier in the epidemic, especially in the Northeast.4, 15, 24
Shooting galleries have exerted an independent effect on the risk of HIV seroconversion
for a decade, which suggests that they may be useful venues for targeted interventions.
A few studies have documented needle-sharing behaviors among shooting-gallery
attendees24-25; however, published
reports of interventions in these settings are lacking.26
We demonstrated only a modest protective effect of methadone maintenance
and NEP attendance on HIV seroconversion, in contrast with earlier reports.27-32
Incidence of HIV was 60% lower among men enrolled in methadone maintenance
compared with men who were not, but this association did not persist after
adjusting for other factors. A possible interpretation for our findings is
that in the presence of sexual risks, measurable effects of interventions
focusing on parenteral transmission will be underestimated. Low power may
have also limited our ability to draw inferences, since 15% of the cohort
members were enrolled in methadone maintenance at any given time, and NEP
was introduced in Baltimore more than halfway through the follow-up period.
We observed that male IDUs who recently engaged in homosexual activity
were more than twice as likely to seroconvert as those who did not. Among
the 69 men who had sex with another man during the study period, HIV incidence
was 10.2% per year. Despite 2 decades of HIV/AIDS research, men who have sex
with men who also inject drugs remain a hidden population of which relatively
little is known.33-34 These men
may experience a dual risk of HIV infection through the sharing of injection
equipment and unprotected anal sex, both of which may be more common among
men trading sex for money or drugs.33, 35
Being a gay male drug user has been closely associated with shooting-gallery
attendance, needle sharing, and HIV positivity.24, 35-37
Our study confirms the elevated risk of HIV seroconversion among male IDUs
who have sex with men and underscores the urgent need to develop effective
interventions for this vulnerable subgroup.
Interestingly, male IDUs who reported not having a heterosexual partner
were more likely to acquire HIV infection, a finding that was not explained
by homosexual/bisexual activity. Similar associations have occurred elsewhere,
which may suggest that high-risk injection practices are more common in the
absence of a partner who can provide social support.14, 38
Lack of heterosexual partnership may also be a marker for more severe drug
dependence.
In contrast, indicators of high-risk heterosexual activity were more
significant than needle-sharing behaviors as independent predictors of HIV
seroconversion among female IDUs. Incidence of HIV was double among women
who reported an STD in the prior 6 months compared with those who did not.
This supports earlier cross-sectional studies, most of which focused on male-to-female
HIV transmission.16, 39-41
Apart from being an indicator of unprotected sex, several common STDs are
cofactors of HIV transmission,40, 42-43
suggesting that NEPs and drug treatment programs, for example, should place
greater emphasis on STD screening and treatment for IDUs. Interventions are
needed to reduce sexual risks among women, eg, couple counseling or promoting
woman-controlled barriers (including microbicides and female condoms). Prevention
programs should take into account the fact that women tend to have greater
overlap between their sex and drug networks than men.23, 44
We did not observe an independent effect of trading sex with HIV seropositivity
after accounting for other sexual risks, which is unlike the observations
in other studies.23, 45-46
A possible explanation is that a higher proportion of commercial sex acts
may have been protected through condom use compared with the sex acts of noncommercial
partners.
Interpretation of our study findings should take into account a number
of limitations. In any cohort, differential losses to follow-up can bias associations
of interest. During the study period, follow-up rates were excellent among
participants who returned at least once, but those who did not return were
significantly younger and more likely to have been homeless,19
suggesting that incidence could have been underestimated. However, compared
with dropouts, subjects who returned were more likely to report frequent injection
and needle sharing at enrollment.19 Therefore,
it is difficult to predict whether our HIV incidence estimates could be biased
upwards or downwards. Caution should be exercised in generalizing our data
to the IDU population in Baltimore or other settings.
With the exception of data on NEP attendance, we relied on self-reports,
which are prone to socially desirable responding.47
Comparing interviewer-administered questionnaire data with audio computer-assisted
self-interviews (ACASI), we recently found that men were more likely to overreport
heterosexual activity to an interviewer, which could explain the inverse association
we observed between HIV seroconversion and number of heterosexual partners.48 Smaller numbers of women may have masked other associations.
On the other hand, because this was a prospective study there is greater confidence
that the drug-related and sexual risk factors we identified were causally
related to HIV seroconversion.
In this cohort of more than 1800 IDUs, HIV incidence declined over time
but remained unacceptably high for a 10-year period. We documented a number
of risk factors for HIV seroconversion that differed significantly by sex.
Although parenteral risks remained important risk factors for HIV seroconversion
among men, those who engaged in homosexual activity were at increased risk
of infection, and sexual risks predominated among women. The extent to which
drug-related and sexual risks contribute to HIV incidence likely depends on
local factors such as social networks, the nature and intensity of interventions,
and the background prevalence of HIV infection among various subpopulations.13, 49-50 Nevertheless, the
HIV risk factors we identified are similar to those described in a recent
report from San Francisco, Calif, where HIV prevalence and incidence among
IDUs has remained low.46 As HIV incidence attributable
to injection drug use decreases (which is the case in New York City50), it can be expected that the relative contribution
of sexual HIV risks will increase. In light of these findings, HIV prevention
programs aimed at IDUs should be sex specific and take into account both sexual
and parenteral risks.
AUTHOR INFORMATION
Accepted for publication November 11, 2000.
This study was supported by grant DA12568 from the National Institute
on Drug Abuse, Bethesda, Md.
Presented in part at the 13th International AIDS Conference, Durban,
South Africa, July 9-14, 2000.
We are indebted to the study participants for their continued participation
in the AIDS Link to Intravenous Experience (ALIVE) study. The authors also
thank study staff, especially Grace Macalino, PhD, and the Baltimore Needle
Exchange Program and evaluation staff for technical support; Roel Coutinho,
MD, PhD, Alex Kral, PhD, and Samuel Friedman, PhD, for critical appraisal
of the manuscript; and Ms Hazel Hamond-Terry for assistance with manuscript
preparation.
Reprints: Steffanie A. Strathdee, PhD, Department of Epidemiology,
Johns Hopkins School of Public Health, 615 N Wolfe St, Room E6010, Baltimore,
MD 21205 (e-mail: sstrathd{at}jhsph.edu).
From the Department of Epidemiology, Johns Hopkins School of Public
Health, Baltimore, Md (Drs Strathdee, Celentano, Vlahov, and Nelson, and Mss
Safaiean Johnson); Ben-Gurion University, Beer Sheeva, Israel (Dr Galai);
and the Center for Urban Epidemiologic Studies, New York Academy of Medicine,
New York, New York (Dr Vlahov).
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