Trends in Sexually Transmitted Diseases and Risky Behaviors Among HIV-Infected Patients at an Outpatient Clinic in Southern Taiwan : Sexually Transmitted Diseases

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Trends in Sexually Transmitted Diseases and Risky Behaviors Among HIV-Infected Patients at an Outpatient Clinic in Southern Taiwan

Lee, Hsin-Chun MD*†‡; Ko, Nai-Ying RN, PHD§; Lee, Nan-Yao MD; Chang, Chia-Ming MD; Liu, Shiao-Ying RN; Ko, Wen-Chien MD†‡∥

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Sexually Transmitted Diseases 37(2):p 86-93, February 2010. | DOI: 10.1097/OLQ.0b013e3181bd8301
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Concurrent sexually transmitted diseases (STDs) in HIV-infected persons are common, either at the time of first diagnosis with HIV or thereafter.1–5 Continued high-risk sexual practices and substance use are 2 major risk factors associated with STD coinfections.1 Individuals with active STDs are more susceptible to HIV infection, and in HIV-infected subjects, concurrent STDs increase cutaneous and genital tract viral concentrations.6 Therefore, early diagnosis, effective treatment of STDs, and reducing HIV-related risky behaviors are important strategies for preventing HIV transmission.6,7

In 2003, the Centers for Disease Control and Prevention of the United States recommended the incorporation of HIV prevention into the medical care of persons living with HIV (PLWH) based on a 3-component strategy: screening for HIV risk behaviors and STDs, behavioral interventions, and partner counseling and referral.8 Growing evidence also indicates that HIV prevention efforts focusing on PLWH are effective in reducing STDs9 and the potential for HIV transmission, with a 36% reduction in risky, transmission-related behavior.10 The fact that antiretroviral therapy-resistant viruses can be transmitted to uninfected persons, which may in turn limit the effects of first-line antiretroviral therapy,11,12 reinforces the importance of “prevention with positives.” Clinical care settings offer opportunities for HIV/STD prevention to HIV-infected patients. Identifying risky sexual and drug-use behaviors among PLWH and using them as the basis for tailoring the prevention strategies are important issues in HIV care.13,14

In Taiwan, HIV-infected individuals have had access to free highly active antiretroviral therapy (HAART) since 1997, and they receive medical care from AIDS referral hospitals. The morbidity and mortality of HIV/AIDS patients in Taiwan have significantly decreased since the introduction of HAART.15 However, the HIV epidemic continues, with a 10% to 32% annual increase in the number of newly reported patients infected with HIV via sexual contact in the HAART era.16 Thus, an understanding of risky sexual behaviors and early detection of concurrent STDs in HIV-infected individuals are important and effective prevention policies. Previously, we found that the seroprevalence rate of syphilis among patients with newly diagnosed HIV infections is 15.5%, and active syphilis accounts for more than half of those individuals who are seropositive for syphilis.17 Another recent study focusing on HIV-infected patients who attended an STD clinic in a metropolitan area in northern Taiwan revealed that 24% of the participants reported an STD diagnosis after receiving a positive HIV test result. Men having sex with men (MSM), having casual sexual partners, and knowing one's positive HIV status for longer than 11 years are independent predictors for unprotected sex.18 Thus, an understanding of the sexual health of HIV-infected individuals is important in designing STD prevention strategies.

The current study attempted to determine the prevalence of concurrent STDs and risky behaviors among HIV-infected individuals in an outpatient clinic.


Study Population and Criteria for Enrollment

The National Cheng Kung University Hospital (NCKUH) is a referral center for HIV/AIDS care in southern Taiwan that has cared for more than 987 patients with HIV since 1992. Until the year 2000, serological tests for syphilis were included in routine examinations at the initial visit for newly diagnosed HIV-infected patients.17 At the follow-up visits for HIV care (usually every 3–4 months), diagnostic procedures for STDs were performed only when a patient presented any symptoms relevant to STDs. Serologically confirmed syphilis triggered a follow-up of serum rapid plasma reagin (RPR) test, every 3 to 6 months after treatment. No periodic STD screening for HIV-infected patients was performed.

HIV-infected patients older than 18 years of age who attended regular follow-ups at outpatient clinics at the NCKUH between August 2005 and December 2005 were invited to participate in this study. HIV-infected inmates (from various correctional facilities in southern Taiwan) who visited our outpatient clinics during the study period were excluded from the study.

Study Procedure and Instruments

Approval for this study was obtained from the institutional review board at NCKUH. Informed consent was obtained from all subjects before data collection.

The prevalence of STDs at the different time points was estimated using 3 different methods: a self-administered questionnaire, a review of the medical records, and active surveillance for STDs (Fig. 1). At study enrollment, active surveillance for STDs (including physical examinations for any mucocutaneous lesions relevant to STDs, serological tests for syphilis, and urine tests for Neisseria gonorrhoea and Chlamydia trachomatis using the polymerase chain reaction) were performed for each participant irrespective of the presence of relevant symptoms or signs. If a participant presented with symptoms relevant to STDs other than syphilis, gonorrhoea, or chlamydial infection, diagnostic procedures were performed according to the decision of the attending physician.

Figure 1.:
Scheme of the study design. The prevalence of STDs at different time points, (I) pre-HIV diagnosis, (II) HIV diagnosis, and (III) study enrollment, were estimated using different methods. STDs indicates sexually transmitted diseases.

We provided a self-administered questionnaire to assess demographic information, sexual orientation, behaviors risky for HIV transmission, past and current STD-related symptoms or diagnoses, and recent sexual behaviors. “Condom use” was assessed by the following questions: “Did you or your sexual partner use a condom during your most recent sexual encounter?” and “Who wore the condom? You, your sexual partner, or both?” All participants completed the questionnaire and provided blood and urine samples on the day of study enrollment. “Newly diagnosed” patients were defined as having a diagnosis of HIV infection within 3 months of study enrollment. “Sexually active” was defined as one or more sexual encounters within 3 months of study enrollment.

Immunologic and virological data, type of concurrent STDs and opportunistic infections at the time of diagnosis with HIV infection, and frequency of STDs since the diagnosis of HIV infection to the time of study enrollment (Fig. 1) were obtained by systemically reviewing the medical records of each participant.

Participants were categorized into 3 at-risk groups: MSM, heterosexuals, and injection drug users (IDUs), according to the presumed HIV transmission routes derived from the information provided by patients and by their medical records. “Heterosexuals” comprised individuals with no history of injection behavior but who acquired HIV infection from opposite-gender sexual partners.

Specimen Collection and Laboratory Procedures

About 10 to 20 mL of first catch urine specimens and 8 mL blood samples, provided by the participants at study enrollment were transported (at room temperature and within 20 minutes) to the microbiology laboratory of the NCKUH for further processing and testing.

Nontreponemal antibodies against Treponema pallidum were measured using the RPR test (RPR Card Test; Becton-Dickinson, Sparks, MD), and treponemal-specific antibodies were measured using the T.pallidum hemagglutination (TPHA) assay (SERODIA-TPPA; Fujirebio, Taoyuan, Taiwan). The RPR and TPHA tests were performed according to the manufacturer's instructions. Participants with a TPHA titer ≥1:160 were considered as T. pallidum-seroreactive.

Each urine sample was stored at 2°C to 8°C in the laboratory before testing, and was then processed by polymerase chain reaction within 7 days of collection. Urine specimens were tested for microbial genetic fragments of C. trachomatis or N.gonorrhoeae using a nucleic acid amplification test (COBAS AMPLICOR assay; Roche Molecular Diagnostics, Branchburg, NJ), according to the manufacturer's instructions.

Statistical Analyses

Statistical analyses were conducted using SPSS, version 11.0 for Windows (SPSS, Chicago, IL). Data were analyzed to determine the statistical significance of differences in demographic characteristics, immunologic and virological status, HIV treatment, rate of concurrent opportunistic infections at the time of HIV diagnosis, STDs at different time points, and recent sexual behaviors for the 3 at-risk groups. Categorical variables were analyzed by using Pearson chi-square test or Fisher exact test if the expected value was less than 5. Continuous variables were analyzed by analysis of variance with post hoc Scheffe tests to determine whether group differences according to age, HIV plasma viral load, CD4 T-lymphocyte count, and duration between HIV diagnosis and study enrollment. Multivariate logistic regression was used to examine the statistical relationship between the presence of active STDs at enrollment and potential correlates, including variables with a P <0.1 in the univariate analyses. A P <0.05 was considered as statistically significant.



During the study period, 395 HIV-infected adults with 1349 outpatient visits for HIV-related medical care were seen at the site. The HIV at-risk groups included MSM (154 patients, 39.0%), heterosexuals (81, 20.5%), IDUs, (156, 39.5%), and unknown risk (4, 1%). After 170 prison inmates were excluded, 123 (54.7%) of the 225 eligible patients participated in the study.

The age of the 123 participants at the time of HIV diagnosis ranged from 19 to 74 years (mean ± SD: 35.1 ± 12.0 years). The distribution, about the 3 at-risk groups, was as follows: MSM, 81 (65.8%); heterosexuals, 29 (23.6%); IDUs, 13 (10.6%). At enrollment, 17 (13.8%) patients had been recently diagnosed with HIV infection, and 98 (79.7%) were receiving HAART. A total of 87.8% had CD4 T-cell counts greater than 200/μL, and 71.5% had a plasma HIV viral load less than 400 copies of RNA/mL (Tables 1 and 2). More individuals in the IDU group (46.2%) had been recently diagnosed as HIV infected at enrollment than in the MSM (13.6%) or heterosexual groups (0%) (Table 1). IDUs had higher mean CD4 T cell counts than those of the other 2 groups at HIV diagnosis. Immunologic status was similar in each group at enrollment because there were more cases being treated with HAART in the MSM and heterosexual groups (80.2%–96.9% vs. 38.5% in IDU, Table 2). The mean duration between HIV diagnosis and enrollment in the IDU group was 13.6 months, which was shorter than those in the other 2 groups (P <0.004).

Demographic, Immunological, and Virological Data Among 123 HIV-Infected Participants for Different At-Risk Groups
Clinical Characteristics and Sexually Transmitted Diseases (STDs) Among 123 HIV-Infected Participants Categorized According to Different At-Risk Groups

History and Types of STDs Before, Concurrent With, and After Diagnosis of HIV Infection

Among the 123 participants, 53 (43.1%) reported a history of STDs before diagnosis of HIV. Syphilis and genital warts were the 2 leading STDs (Table 2). The MSM group was more likely to report a history of STDs than the other 2 groups (53.1% vs. 31% and 7.7%, P = 0.003).

A total of 43 participants (36.1%) had concurrent STDs at the time of HIV diagnosis: syphilis (28 cases of latent syphilis and 4 cases of secondary syphilis), genital warts (9), genital herpes (5), and chlamydial infection (1) (data not shown).

Of the 123 patients, 24 (19.5%) had experienced 31 new episodes of STDs since the diagnosis of HIV infection. Of the 31 episodes, 25 (80.6%) occurred in the 21 participants who had been aware of their HIV status for more than 3 months. The types of new STD episodes were secondary syphilis (16 episodes), genital warts (6), latent syphilis (4), chlamydial infection (3), gonorrhea (1), genital herpes (1), and molluscum contagiosum (1). Patients in the MSM group were more likely to have had one or more new episodes of STDs than patients in the other groups (22/81, 27.2% for MSM vs. 2/42, 4.8% for the others, P = 0.003). By the time of enrollment, the proportion of cases remaining free of STDs since the diagnosis of HIV infection was lower in the MSM group than in the other 2 groups (Fig. 2, P <0.028).

Figure 2.:
Proportion of individuals free of newly diagnosed sexually transmitted diseases since HIV diagnosis according to different risk groups. STD indicates sexually transmitted disease; MSM, men having sex with men; IDU, intravenous drug users.

Syphilis was the most common type of STD among the HIV-infected participants according to the self-reported STD history before HIV diagnosis (about 7/10), at the time of HIV diagnosis (32/43, 74.4%), among new episodes of STDs since the HIV diagnosis (20/31, 64.5%), and at enrollment (7/11, 63.6%). Most of the participants with active syphilis were MSM.

Concurrent STDs at Enrollment and Sexual Behaviors

A total of 11 (8.9%) of the 123 participants, exclusively in the MSM group, had active STDs at enrollment. Of these 11, 8 had related symptoms. There were 5 cases of latent syphilis, 1 of secondary syphilis, 1 of neurosyphilis, 3 of chlamydial infection, and 1 of anal condyloma.

More than half (55.3%) of the participants had experienced their last sexual encounter within 3 months of enrollment (Table 3). Fewer than half (46.3%) reported having sex with their regular partners. The MSM group (64.2%) was more likely to have had sex with casual partners than the other groups (P = 0.005). The rate of condom usage during the most recent sexual act was 68.3%, and a significantly lower frequency of condom usage was found among the participants who had participated in sex with casual partners (57.6% vs. 80.7%, P = 0.006). Of the 32 patients who reported having had anal sex, 15.5% did not use condoms. The overall rate of illicit/recreational drug use in association with sex was 7.9%, and 14.3% used sex enhancers. No association between drug use (using either illicit/recreational drugs or sex enhancers) before sex and condom use was detected (P = 0.592).

Information On the Most Recent Sexual Behavior of the 123 Participants, by Risk Group

Participants recently diagnosed with HIV infection more frequently presented active STDs at enrollment (35.3% vs. 4.7%, P = 0.001) and had used sex enhancers more often during the latest sexual act (35.7% vs. 11.2%, P = 0.029) than those in the other group.

Predictors of Active STDs at Enrollment

Univariate analysis identified younger age, MSM, HIV diagnosis within 3 months, and a history of repeated STDs since HIV diagnosis as being correlated with having active STDs at enrollment (Table 4). Sexual behaviors during the most recent sexual intercourse (including nonuse of condoms, casual partners, specific types of sexual practices, and drug use) did not predict the presence of active STDs at enrollment. In multivariate logistic regression analysis adjusted for age, HIV diagnosis within 3 months (odds ratio [OR], 46.5; 95% confidence interval [CI], 3.9–552.0; P = 0.002), and repeat STD history since the HIV diagnosis (OR, 18.7; 95% CI, 1.7–201.6; P = 0.016) were independent predictors for participants presenting active STDs at enrollment. While nonuse of condoms was included in the multivariate analyses, concurrent STDs at HIV diagnosis was found to be associated with a significant risk of presenting active STDs at enrollment (OR, 8.2; 95% CI, 1.1–58.6; P = 0.037).

Predictors for Active Sexually Transmitted Diseases (STDs) at Enrollment Among 123 HIV-Infected Participants


Our results revealed that more than half (55.3%) of the HIV-infected participants were sexually active in the previous 3 months, and the rate of condom usage during the most recent sexual encounter was 68.3%. A total of 8.9% were confirmed to have active STDs. These findings are consistent with reports from other countries in the past decade.2,19–21

We found the prevalence rates of STDs before and at the diagnosis of HIV to be approximately 40%, and syphilis was the most common type of STD. These findings echo a recent report in the United States demonstrating that 23.1% of newly diagnosed HIV-infected individuals have a concurrent STD and that early syphilis confers the greatest risk (OR, 11) for newly diagnosed HIV.3 Although the prevalence of STDs at study enrollment was only 8.9%, a substantial proportion (19.5%) of the participants had experienced one or more episodes of STD after the diagnosis of HIV had been made, and this phenomenon was more common in the MSM group than in the other 2 groups. A history of repeated STDs after diagnosis of HIV infection was an independent predictor for active STDs. These findings demonstrate that STDs frequently occurred even in patients aware of their HIV-infected status4 and highlight the need to continue behavioral intervention and periodic rescreening for any new STDs after a sexually transmitted infection,22 specifically targeting HIV-infected individuals with STDs.

From our data, most of the participants with active syphilis were MSM. In the past 10 years, outbreaks of syphilis among MSM have been noted in many cities in the United States, Europe, and Australia.23–26 A recent epidemiologic study of men diagnosed with primary and secondary syphilis at STD clinics in 3 US cities revealed an HIV incidence of 10.5% per year, which is higher than that observed in other populations of MSM (3%–4% per year), further implicating an influence of syphilis on HIV incidence among MSM.27 In Taiwan, epidemiologic information on syphilis about different sexual practices is not available in the current reporting system. The syphilis trend in a specific population, such as the MSM group (which is also a major HIV-risk group in Taiwan), requires further clarification. Combining these recent results with our earlier findings for gay bathhouses in Taiwan (showing that individuals with seroreactivity to TPHA have a seven-fold risk for HIV infection),28 the present findings suggest that we should be concerned about the impact of syphilis on the HIV epidemic among MSM.23,25,27

The association of recreational drug use and unsafe sex with an increased risk for HIV and other STDs has been observed in many studies.29–32 Our study did not, however, demonstrate the association between drug use before sex and the nonuse of condoms, which is probably related to limited cases in our study. In addition, potential drug–drug interaction between illicit/recreational drugs and antiretroviral therapy is another health concern among HIV-infected individuals.33 However, information about the use of these drugs was rarely recorded in medical charts. According to our earlier study, 11% of gay bathhouse clients reported a history of recreational drug use, which was also identified as an independent predictor for HIV infection.28 The interaction between drug use and risky behaviors, and the impact of drug use on HIV/STD transmission, should never be overlooked.

The strength of our study is its description of current STD trends before and after diagnosis of HIV infection. This approach provided an opportunity to observe the scope of STDs among HIV-infected individuals at different stages of their lifetime encounters with HIV. The results indicate that STD prevention and treatment efforts should not only be a component of HIV medical care, but should also be implemented early in HIV prevention strategies.

The current study had several limitations. First, a large proportion (up to 90%, data not shown) of the HIV-infected IDUs in the study hospital was incarcerated in correctional institutions, and their exclusion limited our sample size. Second, individuals in Taiwan are accustomed to obtaining medical help for possible STDs from private clinics or treating themselves by taking medicines available in drug stores. The frequency of repeat STDs in HIV-infected patients might have been underestimated due to the use of information available only in reviews of the medical charts. In contrast, overestimation of the rate of STDs might also be a problem because of the latent/reactivated nature of many STDs. Third, the design of the questionnaire did not include elements about the consistency and correct usage of condoms during sex. In addition, syphilis was the most common active STD in our study population. As a venereal disease that is highly contagious via mucosal contact, condom effectiveness for its prevention at an individual level may depend on whether the mucosal site is covered by the condom. Lack of this detailed information may conceal an association between not using condoms and the risk of active STDs. Fourth, use of different methodologies for measuring STD prevalence at different time points could preclude comparison of our data. Carefully interpreting the epidemic trend of STDs will provide more precise information for designing prevention strategies.

In summary, HIV-infected individuals demonstrated a high rate of concurrent STDs either before or at the time of diagnosis with HIV infection and remained sexually active after learning of their positive HIV status. Having a newly diagnosed HIV infection, concurrent STDs at HIV diagnosis, and a history of repeat STDs since HIV diagnosis were independent predictors for active STDs. These predictors are the targets of HIV/STD prevention efforts, and a more effective prevention strategy is needed to reduce the occurrence of syphilis.


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