Known high-risk behaviors for sexually transmitted infections (STI) include having multiple sexual partners and sex without use of condoms. The use of illicit and recreational drugs has been found to be associated with these behaviors1–11 and STI.12–19 Previous studies assessing the relationship between drug use and STI focused only on women12,13 or men having sex with men (MSM),17,18 on one type of drug,13,18,19 or on only one STI.14,15,17
In the Netherlands, the use of various drugs in the general population stabilized between 2001 and 2005.20 However, the use of XTC (3–4 methylenedioxymethamphetamine) is higher compared with other European countries, and the use of GHB (γ-hydroxybutyric acid) has increased in recent years.20 Because the Netherlands has a liberal drug use policy, questions regarding such use are less sensitive here than in other countries. Thus, self reports may be more reliable, providing a unique opportunity to investigate the association between sex-related drug use and STI.
We hypothesized that drug use just before and during sex is associated with STI because it increases high-risk sexual behavior. In a cross-sectional study among clients of a large STI outpatient clinic of the Public Health Service of Amsterdam, the Netherlands, we assessed the prevalence of recreational drug use during sex and whether recreational drug use during sex was associated with STI (chlamydia, gonorrhea, and/or syphilis). Finally, we assessed whether drug use during sex was associated with STI after adjusting for demographics and high-risk sexual behavior. We assessed this separately for heterosexual men, MSM, and women visiting the STI clinic.
MATERIALS AND METHODS
The outpatient STI clinic of the Public Health Service of Amsterdam (GGD Amsterdam) offers free and anonymous STI testing and treatment. In 3 waves—April 2008, October and November 2008, and April 2009—consecutive new attendees of the clinic were asked to participate, totaling approximately 1000 attendees per period. This was done in the course of a long-standing biannual anonymous survey among STI clinic clients, originally started to monitor HIV prevalence.21 The inclusion criteria were consecutive new attendee visiting the clinic for STI screening, an age of 16 years or more, and a sufficient understanding of Dutch or English. After the routine consultation with the nurse, the study was explained, and the client was invited to participate. After written informed consent was obtained, trained interviewers asked about sociodemographics, sexual behavior, and drug use. The medical ethics committee of the Academic Medical Center approved the study.
Procedures and Laboratory Testing
According to the standard protocol of the STI outpatient clinic at the GGD,22 heterosexual male clients were screened for gonorrhea and chlamydia. All MSM were screened for urethral chlamydia and gonorrhea, for anal and pharyngeal gonorrhea, and, if receptive anal sex was reported, for anal chlamydia. Women were screened for cervical and urethral chlamydia and gonorrhea and anal gonorrhea. If oral sex was reported, they were tested for pharyngeal gonorrhea, and, if anal sex was reported, for anal chlamydia. All clinic visitors were tested for syphilis and HIV (unless they actively refused or were known to be infected).
To diagnose chlamydia and gonorrhea, a nucleic acid amplification test (Gen-Probe Aptima Combo 2 Assay, Gen-Probe Incorporated, San Diego, CA) was used.
Serum testing for syphilis was performed for all attendees with the Treponema pallidum particle agglutination assay (Fujirebio, Tokyo, Japan); when reactive, the rapid plasma reagin card test (RPR nosticon II, Biomérieux, Marcy l'Etoile, France), the fluorescent treponemal antibody absorption test (Trepo-spot IF, Biomérieux, Marcy l'Etoile, France), and the Venereal Disease Research Laboratory test (Wellcome, Dartford, United Kingdom) were performed to confirm and classify the infection.
As part of the survey protocol, all participants were screened anonymously for HIV antibodies by means of a third-generation, commercial, microparticle enzyme immunoassay system (AxSym HIV Ag/Ab Combo, Abbott, Abbott Park, IL). Positive test results were confirmed by immunoblot (INNO-LIA HIV I/II Score; Innogenetics N.V., Ghent, Belgium).
Demographics, Sexual Behavior, and Drug Use
Men were classified as MSM if they reported having had sexual contact with a man in the previous 6 months. Ethnicity was defined according to Statistics Netherlands (CBS)23 on the basis of country of birth and maternal or paternal country of birth. The reference period for reported sexual behavior, number of sexual partners (steady and casual), and drug use (cannabis, XTC, “poppers” [alkyl nitrites], heroine, cocaine, GHB, apomorfine, amphetamine, methylamphetamine, mushrooms [psilocybin], ketamine, and explosion [methylone]) was the 6-month period preceding the visit date. If participants reported use of a specific drug, the follow-up question was “Have you used this drug just before or during sexual activities?”
Educational level was divided into 2 categories: low educational level (no education, primary school, lower general secondary education, or lower and intermediate vocational education) and high educational level (higher general secondary education, preuniversity education, higher vocational education, university education, or PhD).
An anonymous database was assembled from routine STI screening data, the survey data, and the laboratory results. Data analyses were performed with Stata 9.2 (Stata Intercooled, College Station, TX). In multivariable analyses, we used different age categories based on interquartile ranges (IQRs) for heterosexual men, MSM, and women to avoid imbalances between age categories. The number of sexual partners was summarized as the median with an IQR. Drugs were omitted from further analyses when <1.5% of participants reported that they had used a specific drug during sex. Amphetamine and methylamphetamine were combined into a single variable “(meth)amphetamines.” Differences between proportions were tested using the χ2 test. We regarded age, ethnicity, and educational level a priori as important possible confounders and forced them in all multivariable models. HIV status was forced into the multivariable model for MSM; the prevalence of HIV in heterosexual men and women was too low to include HIV into the multivariable model. We defined 4 high-risk behaviors: (1) ≥2 steady partners; (2) ≥2 or ≥6 casual partners (≥2 for heterosexual men and women, ≥6 for MSM); (3) unsafe vaginal sex (sex without the use of condoms); and (4) unsafe anal sex. We performed logistic regression to assess associations between sex-related drug use and STI for each specific drug or for “any drugs” used during sex, with demographics as confounder and also including high-risk sexual behaviors. High-risk sexual behavior variables that were significant at P < 0.25 in the univariate model were included in the multivariable model and retained in the model when significant at P < 0.05 in the multivariable model. If the variables regarding sex-related drug use were not significant in the final model adjusted for demographics and sexual behavior, we concluded that the sex-related drug use was associated with STI through sexual behavior. If, however, in the final model, variables regarding sex-related drug use, despite adjustment for demographics and relevant sexual behavior, were still significantly associated with the outcome (i.e., any STI), we concluded that these drugs may have an independent effect on the acquisition of STI, unrelated to the reported sexual behavior. Additional stratified analyses were performed for HIV-negative and HIV-infected MSM.
All interactions between sex-related drug use and high-risk sexual behavior variables retained in the final model were checked. Results were expressed as odds ratios (OR), with 95% confidence intervals (CIs).
A total of 4407 patients of the STI clinic were invited to participate in the study, and 3015 agreed and were interviewed. We compared those who participated with the 1392 who did not in terms of sex, age, ethnicity, and STI complaints and prevalence. Heterosexual males and people with a non-Dutch ethnicity were significantly less likely to participate (P < 0.001). The latter may be partly because persons who could not understand Dutch or English were excluded. Clients with an STI diagnosis were more likely to refuse (P = 0.037). There were no other significant differences between participants and nonparticipants. To ensure that all participants in our study population were unique individuals, we excluded 159 participants from further analyses (34 heterosexual men, 76 MSM, and 49 women) who reported in wave 2 or 3 that they had participated in the survey before. Additionally, we excluded 34 patients who reported no sexual partners in the 6 months preceding the study visit, leaving 2822 participants in the analysis.
The median age of the total population was 28 years (IQR, 23–37 years) (Table 1), 1610 (58.0%) were Dutch, and 2026 (72.0%) had a higher education. Of the participants, 673 (23.9%) were MSM of whom 26.4% were HIV infected. HIV infection was rare in heterosexuals (0.3% in heterosexual men and none in women). Most participants had at least 1 casual sex partner in the previous 6 months. MSM had more casual sex partners in the previous 6 months than either heterosexual men or women (both, P < 0.001).
Recreational drugs were used by 1444 (51.2%) in the preceding 6-month period, of whom 754 (52.2%) reported drug use during sex (Table 1). MSM especially reported sex-related drug use (51.6%); poppers, XTC, and cannabis were used most often, with frequent use of cocaine and GHB. HIV-infected MSM report more sex-related drug use (70.6%) than HIV-negative MSM (44.5%, P < 0.001). Women (16.0% reporting sex-related drug use) and heterosexual men (22.6% reporting sex-related drug use) used cannabis, cocaine, and XTC most often. Injecting drug use in this population was rare: 2/2822 reported injecting drug use in the preceding 6-month period.
At least 1 of the 3 STIs (chlamydia, gonorrhea, or syphilis) was diagnosed in 420 (14.9%) of the participants (Table 1). STI was significantly more common among MSM than among heterosexual men or women (both, P < 0.001). Across groups, chlamydia was the most common STI and was diagnosed more often in heterosexual men (P = 0.018) and MSM (P = 0.003) than in women. Gonorrhea and syphilis were rare among both heterosexual men and women. Table 2 shows the prevalence of drug use, age, ethnicity, educational level, and certain types of high-risk sexual behavior by STIs, for each of the 3 groups.
Associations Between Drug Use During Sex, Sexual Behavior, and STI
Sex-related drug use was significantly associated with 3 of 4 high-risk sexual behaviors: ≥2 casual partners and unsafe vaginal and anal sex (data not shown). Sex-related drug use (any drugs and cannabis, XTC, cocaine, or GHB) was neither associated with STI in univariate nor in multivariable analysis (Table 3).
Men Who Have Sex With Men.
In MSM, drug use was significantly associated with 3 of 4 high-risk sexual behaviors: ≥6 casual partners and unsafe active and passive anal sex (data not shown). Both high-risk sexual behavior and sex-related drug use were associated with STI (Table 3). The OR of any drug use and poppers use were reduced from 2.2 to 1.5 and from 2.3 to 1.7, respectively, after adjusting for demographics, HIV status, and high-risk sexual behavior, but it remained significant. There were no significant interactions between the variables of sex-related drug use and the number of casual partners or unsafe anal sex.
We performed additional analyses separately for chlamydia, gonorrhea, and syphilis (data not shown). After adjusting for demographics, HIV status, and high-risk sexual behavior, the ORs of most variables regarding sex-related drug use during sex were no longer significant for chlamydia and syphilis. However, for gonorrhea, the OR of poppers use was reduced from 2.7 to 2.2 (95% CI: 1.3–3.8), but it remained significant (P = 0.002).
Additional analysis stratified by HIV status showed that sex-related drug use was associated with high-risk sexual behavior in HIV-negative MSM, but not in HIV-infected MSM, and that poppers use was associated with STI in HIV-negative MSM (adjOR: 1.7, 95% CI: 1.0–2.8), but not in HIV-infected MSM (adjOR for poppers use: 1.7, 95% CI: 0.9–3.4).
In women, drug use during sex was significantly associated with 2 of 4 high-risk sexual behaviors: ≥2 casual partners and unsafe anal sex (data not shown). Any drug use was neither significantly associated with STI in univariate nor in multivariable analysis (Table 3). None of the 4 variables of high-risk sexual behavior were associated with STI. Women who used GHB or XTC during sex were more likely to have an STI in multivariable analyses adjusting for demographics; high-risk sexual behavior had no independent association with STI in these models (adjOR for XTC use: 2.3, 95% CI: 1.1–4.9 and adjOR for GHB use: 4.0, 95% CI: 1.5–10.8).
We performed additional analyses separately for CT. None of the 4 variables of high-risk sexual behavior were associated with CT. After adjusting for demographics, XTC use and GHB use were independently associated with CT (adjOR for XTC use: 2.6, 95% CI: 1.2–5.4 and adjOR for GHB use: 4.5, 95% CI: 1.6–12.2).
To our knowledge, this is the first study to explore the association between recreational drug use during sex and sexual behavior and the 3 most prevalent bacterial STI (chlamydia, gonorrhea, and syphilis), in heterosexual men, MSM, and women.
This study shows that sex-related drug use in the preceding 6-month period was common and was associated with high-risk sexual behavior in clients of the STI clinic in Amsterdam. The most important findings of this study are that sex-related drug use was associated with STI in women and MSM, but not in heterosexual men. Moreover, drug use during sex in MSM (notably poppers) was associated with STI, even after adjusting for high-risk sexual behavior. Analyses stratified by HIV status showed that sex-related drug use was not associated with STI in HIV-infected MSM. In HIV-negative MSM, sex-related drug use (reported by 44.5%) was associated with STI, even after adjusting for sexual behavior.
It is known that drug use is associated with increased high-risk sexual behavior. This has been shown for injecting drug users,2,4 MSM,5,11 patients seen in an STI clinic,3,15 and young adults who routinely engage in nightlife.1 High-risk sexual behaviors associated with drug use and identified in these studies were an increased number of sexual partners,1,2,15 unprotected anal intercourse,5,11 and no condom use.3 In our study of STI clinic visitors, we found associations between high-risk sexual behavior and recreational drug use.
We assessed whether drug use led to high-risk sexual behavior and STI after adjusting for sexual behavior in 3 separate groups: heterosexual men, MSM, and women. We expected that the association between drug use and STI would decrease or disappear when we adjusted for sexual behavior, as we hypothesized that drug use is associated with STI through increased high-risk sexual behavior. However, this analysis could be performed in only MSM because drug use during sex was not associated with STI in heterosexual men, and sexual behavior was not associated with STI in multivariable analyses in women. In MSM, poppers use during sex was indeed associated with STI through sexual behavior because the OR of poppers use was reduced after adjusting for sexual behavior. However, the use of poppers during sex remained significantly associated with STI after adjusting for sexual behavior, suggesting that poppers use by MSM may lead to STI through different mechanisms. First, drug use could be a surrogate marker for other demographic factors that have an association with STI. However, after we adjusted for demographic factors, such as age, ethnicity, or educational level, in multivariable analyses, use of poppers remained a significant factor. Second, a conceptual model by Drumright et al24 states that drug use leads to altered mental states or loss of muscle control (e.g., GHB25), enhanced sexual function or increased sexual desire (e.g., (meth)amphetamines26), and decreased sensation of pain (e.g., poppers27). Besides decreased condom use and an increased number of sexual partners, these drug effects could lead to an increased number of sexual acts, increased duration of sexual activity, and increased tissue damage, blood–blood contact, and blood–semen–vaginal fluid contact. Third, there might be a direct biologic effect of poppers on STI acquisition, as has been shown for other drugs.28,29 Consequently, the use of poppers during sex could increase STI acquisition.
A strength of the current study is that it contains detailed information about various sexual behaviors in relation to particular drugs used during sex. Because the Netherlands has a liberal drug-use policy and drug use is often openly discussed, reported use by our study participants may be more reliable than in studies conducted elsewhere. A limitation of this study is that we did not enquire about some factors that may have an important role in the transmission of STI: the number of sexual acts in the preceding 6-month period, the duration of sexual acts, and tissue damage or vaginal and anal bleeding during sex. Also, there is the possibility that when sex-related drug use is positively associated with one STI, and negatively associated with an other STI, the net result for the association between sex-related drug use and “any STI” may be that there is no association. However, additional analyses for MSM showed that there were no drugs that were negatively associated with chlamydia, gonorrhea, or syphilis. Some participants may have felt uncomfortable answering detailed questions about their sexual practices and drug use. Because the questions were related to the preceding 6-month period, recall bias may have occurred. In addition, response bias could have occurred because heterosexual males and those with STIs were less likely to participate. This may have led to over- or underestimation of the association of sex-related drug use and high-risk sexual behavior and STI. Another limitation of the study is that the analytical power may be inadequate to demonstrate associations between drug use and STIs in some of the subanalyses, for example, among HIV-positive MSM. Finally, we could not examine dose–response relationships between drug use and STI.
In conclusion, we found a high prevalence of drug use during sex among STI clinic attendees, ranging from 16.0% in women to 51.6% in MSM. We demonstrated the association between sex-related drug use and high-risk sexual behavior in heterosexual men, MSM, and women and the association between sex-related drug use and STI in women and MSM. In MSM, drug use impacted on the risk of STI through high-risk sexual behavior for most drugs. However, poppers use was associated with STI, even after adjusting for sexual risk behavior, indicating an independent effect of poppers use. This effect appeared to be limited to HIV-negative MSM. In HIV-infected MSM, drug use was very common, as were STIs, but drug use was not associated with STI. More research is needed to explore in depth the relationship between drug use (especially poppers) during sex, high-risk sexual behavior, HIV status, and STI. Prevention measures that targeted at decreasing sex-related drug use may decrease the incidence of STI.
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