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Gender Differences in Risk Behaviors Among HIV+ Persons With an IDU History: The Link Between Partner Characteristics and Women's Higher Drug‐Sex Risks

GOLLUB, ERICA L. DrPH*,†,‡; REY, DOMINIQUE MD‡,§; OBADIA, YOLANDE MD‡,§; MOATTI, JEAN‐PAUL PhD; THE MANIF 2000 STUDY GROUP

Original Articles

Background and Objectives:: Risk‐taking behaviors differ among women and men injection drug users (IDU).

Goal:: To specify the nature of sexual and drug risk‐taking among women IDU and ex‐IDU and how it relates to partner characteristics.

Design:: A cross‐sectional analysis of 324 HIV+ subjects enrolled into a prospective cohort study in Marseille, France.

Results:: Women, as compared with men, were considerably more likely to report nonuse of condoms with a main partner (31% versus 12%). They were more likely to shoot with a partner at last injection (39% versus 12%), but far less likely to sterilize used needles (4% versus 16%). Two thirds of both men and women reported consistent condom use with a seronegative partner, but only 47% of men and 23% of women reported the same with a seropositive partner. Among the women only, needle and syringe sharing was associated with consistent use of a condom.

Conclusions:: Women reported behaviors which protect their partners from STD infection more frequently than behaviors which protect themselves. Greater attention must be paid to sexual risk‐taking among HIV+ women.

*From Philadelphia Department of Public Health, Philadelphia, Pennsylvania, †Columbia University School of Public Health, New York, New York, ‡INSERM Research Unit 379, §Regional Center for Disease Control (ORSPACA), Marseille, France

The Manif 2000 Study Group includes: A. Bourgeade, P. Carrieri, J.P. Cassuto, P. Cavailler, M. Chesney, T. Coates, P. Dellamonica, M. Dugourd, P. Dujardin, N. Escaffre, H. Gallais, J.A. Gastaut, E. Gollub, G. Lepeu, A. Loundou, V. Maslin, D. Mechali, J.P. Moatti, Y. Obadia, D. Rey, C. Reynaud‐Maurupt, C. Rouzioux, A. Schaeffer, A. Sobel, C. Tamalet, F. Tremolieres, and D. Vlahov.

The authors thank Carole Giovannini for her expert help in data management and Anderson Loundou for his invaluable program support during data analysis.

This research was supported by the Franco‐American Commission for Cultural Exchange, ANRS (France), ECS ‐ Sidaction (France), and Departmental Council (Bouches du Rhône ‐ France).

Correspondence: Erica L. Gollub, DrPH, Penn/VA Center for Studies of Addiction, University of Pennsylvania, 3900 Chestnut Street, Philadelphia, PA, 19104.

HETEROSEXUAL TRANSMISSION and injection drug use are two important causes of HIV infections among women in France, as in many other countries. Women represent 17.4% of all French AIDS cases,1 but 31% of recently diagnosed HIV cases in the Provence‐Alpes‐Cotes d'Azur (PACA) region.2 Whereas IDU accounts for 28% and heterosexual sex for 62% of 1996 AIDS cases among all French women, in the PACA region, IDU is a more important risk background for AIDS (48%).3

Women's biologic disadvantage vis a vis HIV infection is known and includes a greater likelihood than men of being infected in a single act of penile‐vaginal intercourse with an HIV+ person4,5 and a greater likelihood of being infected with other STD's‐cofactors for HIV infection6,7‐coupled with a lesser likelihood of having symptoms. Women with IDU histories and STD clinic patients report a higher frequency of STD than men, especially untreated STDs.8,9

In addition to biologic vulnerability, women IDU are also at enhanced risk of (re)infection by HIV/STD because they are not financially independent and/or are often caretakers for their families, rendering them a distinct hard‐to‐reach group. Women are thus more likely to engage in sex trade10,11 and less able to insist on condom use during sex.12–15 Women appear to be more likely to be initiated into injection drug use by their male partners16–18; several epidemiologic studies have shown that women are more likely to have drug‐using (and HIV+) partners than men.17–20 Furthermore, IDU women are more likely than men to have unprotected sex with multiple sex partners,20–22 more likely to share injection equipment,23–25 and less likely to clean used works.26 This raised two main questions of interest for the current analysis. First, how does the probability of having a risky partner and gender‐specific drug/sex behaviors interact, if at all, in women's risk? This would be the case if, for example, women practiced different behaviors according to certain partner qualities (such as HIV‐infected or not), whereas men's behavior did not vary. Some studies point to the importance of partner serostatus as a predictor of condom use,27,28 but few have included enough women to make gender comparisons. Second, does gender modify the connection between drug risk‐taking and sexual risk‐taking for an individual? A few relevant data are available, with some studies supporting the hypothesis of a “risk‐taking” personality29 and others not.27 Again, few studies have been capable of analyzing by gender.

This report discusses cross‐sectional data analyzed on the first 324 men and women enrolled in a cohort of HIV+ individuals whose infection was attributed to injection drug use. The retrospective reports of these subjects allowed us to examine risk behaviors in detail, with particular attention to gender differences.

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Subjects and Methods

Since November 1995, continuous enrollment of HIV seropositive men and women with IDU histories into a longitudinal study has occurred in 12 French centres in the Provence‐Cote d'Azur and suburbs of Paris regions of France. Eligible subjects are those whose HIV infection is attributed to injection drug use (IDU) and who are still at an early stage of the illness (Stage A or B according to CDC criteria, and having had a CD4 count of over 300 μL in the past 6 months). For the purposes of this report, subjects are administered a face‐to‐face interview by a counselor, which includes information on partner's drug use and HIV serostatus; in addition, subjects complete a self‐filling questionnaire of approximately 85 items, including detailed questions on the subject's sexual and drug‐related risk behaviors.

For this analysis of male‐female differences in sex and drug‐use risk behaviors, we first tabulated the frequencies of these risk behaviors, including current drug use status, use of shared equipment, cleaning (of paraphernalia) practices, risky sexual partners, protective behavior such as condom use, STD histories, etc. Then, the relationships between partner characteristics, drug risk behaviors, and sexual behaviors, across gender, were evaluated using univariate analyses. Finally we ran separate logistic regression (SPSS, version 6.0) models by gender to assess predictors of our outcome variable, consistent condom use with the main partner in the previous (to intake) 6 months. Both forward stepwise and backward elimination procedures were used to determine the best model.

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Results

Data on a total of 221 men and 103 women, enrolled through April 1997, were available for analysis. Table 1 tabulates general demographic and risk characteristics of interest. The mean age of these subjects was in the low‐mid 30s. Most reported living with or having a main partner, although this was more common among women. Among women who knew about their partner's drug use, the proportion of women with IDU partners (past or current) was more than twice that of men. Women were also more likely to have seropositive partners.

The self‐reported STD and behavioral data point to a higher risk of reinfection for women via the sexual route with HIV or other STD's than the men. Women were nearly three times more likely to report an STD over the past 6 months (13.7% of women, p = 0.01). Nearly three times as many women reported never using a condom with the main partner over the previous 6 months (p = 0.00), and nonuse of condoms was seen more frequently among women using birth control pills (66% versus 37%, p = 0.03). More than one quarter (26%) of the women reported having had anal sex over the past 6 months, of which 32% was condom‐protected.

There was a strong association (p = 0.01) for women between serostatus of the partner and frequency of condom use over the past 6 months, although men as well showed differences in behavior across partner serostatus. Very high and equal proportions of both men and women (73‐76%) reported always using condoms with seronegative partners or with partners whose serostatus was unknown (see Table 2). In contrast, women were half as likely as men to report consistent condom use with seropositive partners in the previous 6 months. An even greater disparity (women 15% condom use with seropositive partners; men 50%) was found on the small subset of subjects who reported that they had stopped injecting (99.4% of whom reported their last injection >6 months in the past; hereafter, “ex‐injectors”), and whose partnerships predated the date of last injection.

Women's drug‐risk behaviors on the whole also indicated a higher level of risk than the men's. There was a strong association between the IDU status (still injecting versus not) of the male partner and the IDU status of women subjects (p = <0.0001). Nearly all (97%) of women and men (98%) who were no longer injecting had partners who also were not current injectors. Women who continued to inject, however, were more likely than men (37% versus 20%) to have partners who also injected. We pooled all women (both current and ex‐injectors) and compared them with the men for analyses of drug risk. Borrowing either a needle or syringe at last injection (which ranged from 1‐20 years preceding entry into the study) was reported somewhat more frequently among women (16.1%) as compared with men (11.9%; p = 0.33). In general, across both sexes, ex‐injectors reported borrowing more frequently than current injectors. As compared with men (15% among ex‐ injectors versus 2% among current injectors), however, this difference in borrowing practices was less pronounced among women (20% versus 7%).

Perhaps the most striking differences concerned behaviors related to cleaning injection material. Overall, only a small fraction (4%) of women, as compared with 16% of the men, reported cleaning their works at last injection, using either boiling, bleach, or alcohol, even though comparable percentages of women and men reported not having new material (Table 1). Most of this difference occurred during injections with the primary partner (which for women were frequent) or by themselves. No women, but 25% of men with a primary partner, reported cleaning used works at last injection when with that partner. Among partnered subjects, 9% of women and 59% of men reported cleaning when alone. Interestingly, however, when shooting drugs with friends, similar proportions of these women and men reported cleaning used works (60% women, 63% men) (data not shown).

We found an overall difference in the interaction between sexual and drug‐use behaviors when comparing men and women. Whether men borrowed a needle or syringe at last injection had no relationship to their condom use practices with a main partner over the previous 6 months, and most were protected (72‐76%). However, for women, not borrowing was associated with a reduced frequency of condom use with a main partner (47% versus 79%) (Table 3). We also found this to be the case when women and men were asked about condom use with any partner and when a different time period was specified, (e.g., last intercourse, whether or not within the past 6 months), however the cell sizes prohibited attaining statistical significance. This association also held for women involved in Methadone programs (data not shown). We then analyzed the serostatus of the partner among those who borrowed. Although the sample size was quite small, the women who borrowed always had seronegative partners, whereas for the men this association did not hold. The seronegative male partners were also more likely to be noninjecting partners (which likely explained the borrowing behavior of the women). These two partner variables were highly associated (p < 0.0001).

Logistic regression analyses confirmed the univariate results (Table 4). We ran separate regression equations for men and for women on the dependent variable consistent use of condoms with main partner over the previous 6 months. For women, four variables had some association with the outcome and were highly interrelated: the HIV status of the partner, the current IDU status of the partner, the subject's borrowing a needle or syringe at last injection, and the subject's IDU status (still injecting versus not). However, in both forward stepwise and backward elimination regression procedures, the best model consisted of the HIV status of the partner (OR = 4.16) and the current IDU status of the partner (OR = 2.73).

For men, consistent condom use was not predicted by any demographic or drug‐use variables in the regression analysis. The only significant predictor, in the same direction as that for women, but with a weaker effect estimate, was the HIV status of the partner (OR = 2.89).

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Discussion

In this cross‐sectional analysis of self‐reported behaviors among persons with an IDU history, we found evidence that suggested that borrowing behaviors have declined over time, in accordance with other work.30,31 We assume that this is related in some measure to outreach efforts on the part of the public health community, such as increased access to clean needles at pharmacies, mobile units, and at automats. In this sample, current IDU reported borrowing needles or syringes at last injection at a much lower frequency than ex‐IDU, and for men the level was negligible. There is still a considerable need for education and needle access for women, however, because 7% of women continue to report borrowing, and of the 34% of women who used dirty works at last injection, only 12% reported cleaning with alcohol, bleach, or boiling. The fact that women reported considerably higher levels of cleaning when shooting with friends suggests that failure to clean with a primary partner, or when alone, was not explained wholly by a lack of knowledge about cleaning techniques.

We found significant differences in drug use and in sexual risk behaviors between HIV+ men and women with an IDU history. Women reported higher rates of STD infection and unprotected vaginal or anal sex. They were more likely to be sexually exposed to reinfection with HIV, as well as infection with other STD agents, as compared with the men, because their main partners were more likely to be seropositive, and because they were more likely to report selling sex for drugs or money. For women injectors, having a partner who did not currently inject offered little protection: most male partners, due to past IDU histories, were HIV+. Women's risk of HIV reinfection and STD infection was further amplified by a systematic lack, as compared with the men, of sexual behaviors which could protect themselves, such as condom use with a seropositive partner. Furthermore, women using oral contraceptives reported a particularly low level of condom use, indicating a need for clarification of contraception and disease prevention and women's dual risks.

Our main findings were two. First, we found a substantial gender difference in the associations between subject's risk behavior and partner's status. For both women and men, reported condom use was associated with the main partner's serostatus, with more consistent condom use reported among those with seronegative partners. This finding corroborates work in other areas of Europe.28,32 In our sample, however, women with seropositive partners reported extremely low rates of condom use, half that reported by the men. Thus, the opportunity for reinfection was high.

Second, for women but not for men, there was a seemingly paradoxical association between borrowing a syringe or needle at last injection and recent use of a condom. Women who borrowed syringes tended to have seronegative partners who were not currently injecting (and who could not provide syringes). One interpretation is that IDU women who borrow syringes or needles are conscious of the sexual risk they pose to their seronegative partners and seek to protect them (and/or that these partners demand a high level of protection themselves), but that protection during sex is not considered important when the partner is seropositive. Both serostatus and injecting status of the male partner appeared to exert a strong influence over the women's self‐protective behaviors. The data do not demonstrate a consistent model of risk‐taking (e.g., risk‐prone versus risk‐averse) for the women. Women were consistent in practicing risky drugsex behavior only when that risk was confined to them‐when it did not compromise the safety of their partner.

There are several limitations to the present analysis. First, the overall sample size was small and there were often very small sample sizes for subgroup analyses, straining the drawing of inferences. For example, only a total of 38 subjects in this analysis reported borrowing a needle or syringe. Therefore, these findings must be considered very preliminary. Second, the data are cross‐sectional and based on selfreport. A recent study, however, found that self‐reported behaviors of IDU agreed well with urine drug analyses.33 Furthermore, currently available data do not allow for time‐concordant analyses of sex and drug behavior. It is possible that the observed associations between drug use and sexual risk behaviors would no longer hold with adequate samples for time‐concordant analyses. Three findings tend to argue against this. First, for other behavioral associations where we did have the capacity to do time‐concordant analyses (for example, in looking at condom use by serostatus of partner) we found that the overall analysis tended to echo the findings of this subgroup analysis. Second, varying the subgroup analyzed (e.g., condom use at last intercourse with any partner, condom use over the past 6 months with main partners only) resulted in a similar gender/behavior interaction, although statistical significance was not attained. Finally, our time concordance problem, in the extreme, may have led us to misclassify subjects' partners' serostatus; although partners were noted as presently seropositive, they may have been seronegative at the time of the reported condom use behavior. As this is more likely to occur with the women's main partners (who were more frequently seropositive), it would tend to increase the gender difference observed.

Over a quarter of the women in this sample reported anal intercourse over the previous 6 months, of which only 50% was condom‐protected. This rate is considerably higher than that found in a French general population survey34 but agrees with US studies of samples where risk of HIV transmission is elevated, such as STD patients35,36 and serodiscordant couples (Nancy Padian, personal communication, December 1997).

The potential implications of these HIV+ women's increased exposure to STD and reinfection are serious. STDs are known co‐factors for HIV infection and, by extension, reinfection. They are likely to aggravate the course of HIV,37 and one consequence of such infection, cervical cancer, is an AIDS‐defining condition. Finally, in the context of increasing rates of failures of new therapies for HIV+ persons,38 reinfection with drug‐resistant strains of the virus will increase in frequency. If this is true, HIV+ women will be selectively disadvantaged, as the probability of any sexually transmitted infection is greater than that for their male counterparts. For all these reasons, redoubled efforts are needed to counsel HIV+ women about the risks of unsafe sex and about methods to reduce their risk during sexual encounters with men, including male condoms, but also female barrier methods, including the female condom.13,15

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