Sexually Transmitted Diseases:
Prevalence of Human Immunodeficiency Virus and Sexually Transmitted Infections and Risky Sexual Behaviors Among Men Visiting Gay Bathhouses in Taiwan
Ko, Nai-Ying PhD†‡; Lee, Hsin-Chun MD*‡; Chang, Jui-Ling BS§; Lee, Nan-Yao MD‡; Chang, Chia-Ming MD‡; Lee, Meng-Ping BS∥; Lin, Yi-Hui BS¶; Lai, Kang-Yen BS#; Ko, Wen-Chien MD*‡
From the Departments of *Medicine and †Nursing, College of Medicine, National Cheng Kung University, Tainan; ‡Department of Internal Medicine, National Cheng Kung University Hospital, Tainan; §Taiwan Love and Hope Association, Kaohsiung; ∥AIDS Care Association, Taichung; ¶Taiwan People Living With HIV/AIDS Rights Advocacy Association, Taipei; and the #Taiwan Tongzhi Hotline Association, Taipei, Taiwan
This study was supported by grants from the Center for Disease Control, Department of Health, Executive Yuan, Taiwan. The authors would like to thank all participants in the study. We are grateful to laboratory staff, including Lin-Wun Mao, Chun-Jing Liang, Hung-Muo Chen, Hung-Ting Liao, and Yu-Ting Chu, and acknowledge Professor Shirley A. Murphy, RN, PhD, FAAN, and Associate Professor Susan J. Fetzer, MBA, RN, PhD, for their reviews of this manuscript.
Correspondence: Wen-Chien Ko, Department of Internal Medicine, National Cheng Kung University Hospital, No. 138, Sheng Li Road, 704, Tainan, Taiwan. E-mail: firstname.lastname@example.org.
Objectives: This study aimed to investigate the prevalence of human immunodeficiency virus (HIV) and sexually transmitted infections (STIs) and predictors of risky sexual behaviors among men visiting gay bathhouses.
Study Design: A cross-sectional study was conducted at 8 gay bathhouses in Taiwan. Bathhouse attendees were invited to complete a questionnaire and to be screened for HIV/STIs.
Results: Of 451 men recruited for the study, 339 (75%) completed the questionnaire and were screened for HIV/STIs. The study indicated that seroprevalence rates of anti-HIV-1 antibody, specific Treponema pallidum antibodies detected by hemagglutination assay, surface antigen of hepatitis B virus, IgG antibodies for hepatitis A virus, antibody for hepatitis C virus, and indirect hemagglutination antibody for Entamoeba histolytica (serum titer ≥1:128) were 8%, 18%, 16%, 38%, 3%, and 6%, respectively. Prevalence rates for chlamydial and gonococcal infections reflected by nucleic acid amplification tests in urine samples were 7% and 4%, respectively. Irregular use of condoms during oral sex, condom inaccessibility at bathhouses, unprotected sex at public venues, no prior HIV test, and 5 or more visits to bathhouses every month were independently associated with unprotected anal intercourse.
Conclusion: Men attending gay bathhouses report engaging in unsafe sex practices and are at substantial risk of acquisition of HIV/STIs. These findings highlight the need for more comprehensive prevention efforts at gay bathhouses.
THE HUMAN IMMUNODEFICIENCY VIRUS (HIV) epidemic in Taiwan continues to grow. The annual incidence rate of reported HIV infections among the general population was 1.6/100,000 in 1997 and 3.7/100,000 in 2003, with an average increase of 15% per year.1 National surveillance data indicated that HIV infections disproportionately affect men having sex with men (MSM). This group accounts for 43% of all reported HIV/AIDS cases and 47% of HIV/AIDS cases among men in Taiwan.2 However, few data on the prevalence of HIV and sexually transmitted infections (STIs) among MSM in Taiwan have been published.
Gay bathhouses have been identified as public venues where MSM are more likely to engage in risky sexual behaviors, such as using party drugs, having multiple sexual partners, and engaging in unprotected anal intercourse.3–7 Gay bathhouses have been the targets of public venues for the transmission of HIV and STIs among MSM.5,6,8 In the early 1980s, for example, studies conducted in Amsterdam, Australia, and Copenhagen reported high prevalences of syphilis, hepatitis B virus (HBV), hepatitis A virus (HAV), and HIV infections among men who frequented gay bathhouses.3,4,9–12 Outbreaks of HAV were reported in gay communities in 1992 in Amsterdam and 1997 in the UK. Visits to bathhouses and darkrooms were significantly associated with HAV outbreaks.13,14 In addition, high prevalence rates of gonococcal and chlamydial infections among men visiting gay bathhouses have been recently reported in Australia.7 Moreover, recent studies reported that early syphilis among MSM of all ages has been on the rise from 1999 to 2003 in major U.S. cities15–18 and other developed countries.19–21 The concerns about the potential increases in HIV transmission among MSM were raised.
No recent studies in Asia have reported HIV/STI prevalence among men who visit gay bathhouses or investigated sexual behaviors that take place in gay bathhouses. The purposes of the current study were to (1) determine the prevalence of HIV and other STIs, including HAV, HBV, hepatitis C virus (HCV) infections, syphilis, amoebiasis, gonorrhea, and chlamydial infection; (2) determine the rates of unprotected sexual behaviors; and (3) identify predictors of HIV infection and unprotected sexual behaviors among male attendees at gay bathhouses. Such information is critical in designing structure-level interventions in gay bathhouses.
Materials and Methods
A cross-sectional study design was used to collect prevalence of HIV/STIs and behavioral data from male attendees at 8 gay bathhouses located in the 3 cities, i.e., Taipei in the northern, Taichung in the middle, and Kaohsiung in the southern part of Taiwan (Fig. 1) during a 3-month period in 2004. In Taiwan, there are at least 20 gay bathhouses; most are located in metropolitan areas. Eight gay bathhouses were selected as study recruitment sites proportionately across the 3 major cities.
The study protocol was approved by the Human Subjects Division Committee of National Cheng Kung University. After getting permission from bathhouse owners, posters were positioned at the entrance desk and public resting areas. The posters displayed messages regarding the purposes, procedures, dates, times, and items of offering HIV/STI screening during study periods. Patrons were approached by male trained volunteers when they checked into the bathhouse and/or they were standing or sitting alone in public areas. Male volunteers approached sauna patrons, introduced the program, and obtained their written informed consent to participate in the study.
Data were collected by trained male volunteers and HIV counselors at each bathhouse every weekend from midnight to early morning (between 10 pm and 2 am), between September and December in 2004. Patrons who agreed to participate were invited to select items of HIV/STI screening listed on the consent form and to complete a 1-page self-administered questionnaire. The HIV/STI screening tests offered included serological tests for HIV, HBV, HCV infections and syphilis at 8 bathhouses across 3 cities. Additional serological tests for HAV infections and amoebiasis, and nucleic acid amplification tests in urine specimens for gonococcal and chlamydial infections, were performed for the participants in middle and southern Taiwan.
The questionnaire included demographic characteristics, gender of sexual partners and sexual behaviors at the latest visit to a gay bathhouse, the place where condoms can be obtained in the bathhouse (accessibility of condom), recreational drug use in bathhouses, the number of visits to a bathhouse in the past 6 months, and venues wherever the participant had engaged in unprotected intercourse. After completing the questionnaire, participants were briefly counseled in private by a trained counselor, and they were screened for HIV/STIs based on the items selected. To improve the validity of participants’ self-reported behaviors, trained HIV counselors double checked each self-administrated questionnaire and clarified those inconsistent answers before conducting HIV/STIs screening tests. Participants were offered a free bathhouse entry ticket and free HIV/STI screening tests as incentives. All HIV/STI screening tests were anonymous. Each participant was given a unique number, which was marked on the blood or urine sample, and a telephone number to report the results between 10 am and 10 pm, Monday through Saturday. Participants with positive results were referred to the nearby hospitals for further clinical management.
Specimen Collection and Laboratory Procedures
Participants provided a first-pass urine or blood sample, depending on their selected HIV/STI tests. The specimens from bathhouses in middle and southern Taiwan were transported to the laboratory of the National Chang Kung University Hospital in Tainan and those in north Taiwan, to the laboratory of Taipei City STD Control Center in Taipei for further processing and testing.
Nontreponemal antibodies to Treponema pallidum were measured by the rapid plasma reagin test (RPR Card Test; Becton-Dickinson, Sparks, MD), and treponemal specific antibodies, by T pallidum hemagglutination (TPHA) assay (SERODIA-TPPA; Fujirebio, Taoyuan, Taiwan). The RPR and TPHA tests were done according to manufacturer’s direction. Participants with a TPHA titer equal to or higher than 1:160 were considered to be T pallidum seroreactive. HIV antibodies were detected by using a single-microparticle enzyme immunoassay (AxSYM HIV 1/2 gO; Abbott GmbH & Co. KG, Wiesbaden Delkenheim, Germany) and confirmed by Western blot (New Lav Blot 1; Biorad, Steenvoorde, France). Serum specimens were tested for IgG antibodies of HAV (AxSYM HAVAB 2.0, Abbott GmbH Diagnostika, Wiesbaden-Delkenheim, Germany), hepatitis B surface antigen (HBsAg), IgG antibodies of hepatitis B surface antigen (HBsIgG) (AxSYM HBsAg [V2] and AUSAB, Abbott GmbH & Co. KG), and antibodies of HCV (AxSYM HCV version 3.0, Abbott Laboratories, Abbot Park, IL). Serum antibodies of Entamoeba histolytica were determined by indirect hemagglutination (IHA) test (Cellognost-Amoebiasis, Dade Behring Marburg GmbH, Marburg, Germany).
Urine samples collected only from bathhouse attendees in middle and southern Taiwan were tested for microbial genetic fragments of Chlamydia trachomatis or Neisseria gonorrhoeae by nucleic acid amplification test (COBAS Amplicor assay; Roche Molecular Diagnostics, Branchburg, NJ), according to the manufacturer’s instructions.
Statistical analyses were conducted using the SPSS 11.0 for Windows software (SPSS, Chicago, IL). Chi-square tests were used to evaluate the association between the positive/reactive result of each HIV/STI and various correlates, including demographic characteristics, illicit drug usage, and risky sexual behaviors. The Fisher exact test was used if an expected value was less than 5. Univariate and multivariate odds ratios and 95% confidence intervals of risk factors for HIV infection were determined by logistic regression. Continuous variables were analyzed by t tests or analysis of variance. Logistic regression was used to examine the statistical relationships between the 2 primary independent variables (unprotected anal intercourse or unprotected oral sex in bathhouses) and significant correlates selected from univariate analysis while controlling for age. Age was entered in the equation first, followed by condom use, condom accessibility in bathhouses, previous HIV testing, the number of public venues used for unprotected sex, and the frequency of bathhouse visit every month. The final model achieved goodness of fit as assessed by the Hosmer-Lemeshow goodness-of-fit test (P = 0.35). P values <0.05 were considered significant.
Characteristics of the Study Participants
Since the exact numbers of bathhouse attendees approached by trained male volunteers were not available, the voluntary participation rate was not available but estimated to be around 80%. A total of 451 men were recruited from 3 cities. Of these, 339 (75%) completed the questionnaire and were screened for HIV/STIs. Seventy (16%) participants responded only the questionnaire, and 42 (9%) obtained HIV/STIs tests and did not complete questionnaires. Responses cannot be added up to a total of 451, because some participants did not answer questions completely (Table 1).
The mean age of the 403 participants answering questions was 33.1 years (SD, 10.5; range, 18–83). The majority of participants (85%) had some college or college degree. Of those, 334 (87%) reported sex exclusively with men, 42 (11%) with both men and women, and 9 (2%) with women. Recreational drugs were ever used in bathhouses by 44 (11%) participants. The most common substances used were ecstasy, nitrites, ketamine, and marijuana. Three hundred seven (76%) men had previously tested for HIV infection. Seven (2%) who had been infected by HIV-1 did not repeat the HIV test but agreed to STI tests. A total of 232 (62%) of 374 participants called for the results of serological examinations, and 127 (84%) of 152 participants called for the results of urine tests.
Prevalence Rates of HIV and Other STIs
The HIV/STI prevalence rates did not differ across bathhouses in 3 cities (Table 2). Only 39 (11%) of 383 men reported STI-related symptoms in the past 6 months, and 155 (41%) of 381 men were tested positive/reactive for at least 1 of HIV/STIs. Overall, HIV-1 infection was newly diagnosed in 31 (8% of 365) men. The prevalence of TPHA seroreactivity was 18% (66/359), and 25 (38%) of 65 men with TPHA seroreactivity had RPR titers equal to or higher than 1:4. Moreover, 81 (38%) of 213 men had been previously infected with HAV, as indicated by the presence of serum HAV IgG. Because all participants were born before 1985 when the national HBV vaccination program for neonates began, none of the participants ever received active immunization by HBV vaccine. Nonetheless, 132 (61%) of 215 had serum HBs IgG, indicating past HBV infection. Fifty-two (16%) of 327 participants had HBsAg detected in serum. The seroprevalence of HCV infections was 3%. Serum E histolytica IHA titers equal to or higher than 1:128 were present in 12 (6%) of 213 men. Of note, the seropositivity rate (9/80, 11%) of amoebiasis was higher in men with past HAV infections than that (3/129, 2%) in those without HAV infections (OR, 5.3; 95% CI, 1.4–20.3). Of 152 urine samples, N gonorrhoeae, C trachomatis, or both were detected in 6 (4%), 10 (7%), or 2 (1%) samples, respectively.
Unprotected Sexual Behaviors at Gay Bathhouses
Bathhouses were reported by 60% of 409 participants as the most common venues for unprotected sex, followed by home (37%), hotels (9%), parks or beaches (5%), gyms (4%), and public restrooms (4%). Unprotected oral sex was a more common sexual practice than unprotected anal sex among gay bathhouse attendees. At the most recent visit to gay bathhouses, more than a half of men (194/334, 58%) self-reported unprotected oral sex, 22% (69/308) had unprotected anal intercourse, and 19% (56/297) practiced both unprotected oral and anal sex. Only 81 men (21%) reported having oral sex exclusively with condom use, and 244 (67%) had anal intercourse exclusively with condom use. Participants reported that the median number of unprotected oral sex at the most recent visit to a gay bathhouse was 1 (range, 0–15); the median number of unprotected anal intercourse was 0 (range, 0–10). Men using recreational drugs in bathhouses were more likely to have more unprotected oral (OR, 2.4; 95% CI, 1.2–4.9) or anal (OR, 15.8; 95% CI, 1.4–178.5) sex partners than men denying use of recreational drugs at each visit to a bathhouse.
Predictors of HIV Infection and Unprotected Sexual Behaviors
In the multivariate logistic regression analysis adjusted for age, HIV infection was independently associated with HCV infection (OR, 21.1; 95% CI, 3.9–112.9), TPHA seroreactivity (OR, 7.1; 95% CI, 2.8–18.3), and previous use of recreational drugs in bathhouses (OR, 3.2; 95% CI, 1.0–10.3) (Table 3). However, attendees’ sexual behaviors occurring at the latest visit to a gay bathhouse did not predict the presence of any HIV/STIs.
In multivariate analysis adjusted for age, 5 factors were independently associated with unprotected anal intercourse at bathhouses: irregular condom use during oral sex (OR, 8.4; 95% CI, 2.5–28.8), the number of public venues at which study participants had unprotected sex (OR, 1.6; 95% CI, 1.1–2.1), 5 or more visits of bathhouse every month (OR, 3.2; 95% CI, 1.5–6.8), condom accessibility in bathhouses (OR, 0.5; 95% CI, 0.3–0.8), and prior tests for HIV infection (OR, 0.4; 95% CI, 0.2–0.8) (Table 4). After adjustment for age, 2 factors were independently associated with unprotected oral sex at bathhouses: irregular use of condoms during anal intercourse (OR, 8.0; 95% CI, 2.8–23.1) and the number of public venues at which they had unprotected sex (OR, 1.7; 95% CI, 1.0–2.7).
The cross-sectional study showed that 41% of gay bathhouse attendees in Taiwan were tested positive or reactive for at least 1 of HIV/STIs, and 8% of gay bathhouses attendees had been infected with HIV, including 31 newly diagnosed cases of HIV infection. Our findings are consistent with 2 recent studies conducted in Taiwan, in which the prevalence rate of HIV infections among MSM was 7 to 9%.22,23 The findings highlight the importance of implementing comprehensive HIV/STIs screening programs in gay bathhouses for early detection of HIV infection and treatment of other sexually transmitted diseases.
Consistent with a survey of sexual behaviors of men who frequented a gay bathhouse in Portland, OR,6 our study found unprotected oral sex was the predominant risky behavior in gay bathhouses. Notably, 79% of men reported inconsistent condom use during oral sex, and 58% reported unprotected oral sex at the latest visit to a gay bathhouse. Subsequently, it is predictable that among male attendees at gay bathhouses, there will be high transmission rates of oral-genital–transmitted diseases, which will increase the likelihood of acquisition of HIV.24,25 In contrast, most (78%) bathhouse attendees in Taiwan did not engage in unprotected anal intercourse, and 67% used condoms consistently during anal sex, and such a sexual precaution was also taken in gay communities in the United States.5,6 The unexpected high percentage of consistent condom use in bathhouse attendees during anal sex was probably related to public education efforts in encouragement of safer sex practices in gay communities, particularly having sex in a high-risk sexual venues. Nevertheless, bathhouse attendees might underreport the risky behaviors, given the pressure of answering private questions in public venues. However, participants’ latest sexual behaviors at bathhouses cannot predict the presence of HIV/STIs. The possible explanation is that HIV/STIs could have been present for some time, and therefore, the latest sexual behavior occurring at bathhouses was not an accurate predictor of HIV/STIs.
The prevalence rate of HAV infections among our participants was 38%, similar to those of the earlier nationwide surveillance data in Taiwan 26–28 but significantly higher than 7% in New Zealand29 and 13.9% in the United States.30 In Taiwan, HAV vaccine has been available, but not mandatory, since 1980. All study participants were born before 1985 (age range, 18–83). Therefore, our study participants with HAV IgG indicated prior infection rather than vaccination. Because HAV infection is sexually transmissible and preventable by vaccination,31 it is important for health care providers to recommend that individuals at risk receive HAV vaccines.
E histolytica infection is a parasitic disease recently recognized among individuals infected with HIV-1 in Taiwan. Of 18 HIV-1–infected males with invasive amoebiasis, 13 (72%) were MSM, consistent with the potential fecal-oral transmission in MSM.22 A significant serum IHA titer of E histolytica was detected in 6% of 213 men in the current study, similar to the seroprevalence rates of E histolytica infection, ranging from 4% to 21%, in earlier studies involving MSM in Japan, Italy, and the United States.22 However, the risk factors or precise transmission modes of E histolytica among MSM remain to be identified. Because both HAV and E histolytica infection can be transmitted via fecal-oral contacts, our data showed that men with prior HAV infections were 5 times more likely to have prior E histolytica infections. Because unprotected oral sex is a common sexual practice in gay bathhouses, our data underscore the need for educating bathhouse attendees regarding the risk for STIs via oral-genital or fecal-oral sex.
The prevalence rate of chlamydial and gonococcal infections among our participants, reflected by nucleic acid amplification tests in urine samples, were 7% and 4%, respectively. These figures were higher than those in a study involving men-only saunas of Australia (1.8% and 0.2%, respectively)7 and those in a MSM cohort study in Pittsburgh (0.2% and 0%, respectively).32 Among MSM, pharyngeal and rectal infections caused by C trachomatis or N gonorrhoeae were often more common than urethral infections.7 Only urine samples were tested, so our data probably underestimated the exact degree of disease burden. Therefore, our study highlighted the importance of STI/HIV surveillance and prevention programs in gay bathhouses and of screening for rectal or pharyngeal infections in future studies.
TPHA seroreactivity, use of recreational drugs, and HCV infection were independently associated with HIV infection in the current study. It is consistent with the notion that syphilitic ulcers facilitate the acquisition and transmission of HIV infection.24,33 As for HCV, it is mainly transmitted by parenteral routes, and thus HCV infections were mainly found in HIV-infected intravenous drug users. However, of our participants, all 9 HCV-infected participants denied intravenous drug use, and after controlling for age and other risk factors, they were 21 times more likely to be infected with HIV than men without HCV infection. Recent studies showed that HCV infection was associated with unsafe sex among HIV-infected MSM, and the risk of sexual transmission of HCV increased in persons with multiple sexual partners, unsafe sex, and HIV-infected MSM.34,35 Consistent with recent studies, our study findings indicate the possibility of interactions between HCV and HIV infections among MSM with high-risk sexual behaviors. The association of recreational drug use and high levels of unsafe sex among men visiting gay bathhouses,5 circuit parties,36,37 and public cruising areas38,39 had been recognized. In the current study, the use of recreational drugs was reported in men with multiple unprotected anal or oral sexual partners and reasonably significantly associated with HIV infections.
There are several limitations of the current study. First, the use of a convenience sample of bathhouse attendees and a cross-sectional study design preclude the generalization of our findings to other MSM communities. Second, the selective participation of motivated volunteers is likely to result in the underestimation of the prevalence of unprotected sexual behaviors. Third, the items of HIV/STI surveys selected by the participants resulted in a potential bias in the estimation of HIV/STIs prevalence. More extensive and rigorous studies with probability sampling and longitudinal designs are needed for future research.
The strengths of this study were its focus on men attending bathhouses across 3 major cities in Taiwan and the collection of both serological and behavioral data. It provided an opportunity to assess the status of HIV/STIs epidemic in a high-risk population. Consistent with previous studies,5,6,8 our study identified several predictors of unprotected anal sex in bathhouses, i.e., previous engagement in unprotected oral sex, unprotected sex in public venues other than bathhouses, frequent bathhouse visits, inaccessibility to condoms in bathhouses, and no prior test for HIV. All these sexual behaviors reflect the ignorance or intentional neglect of the risk of acquisition of HIV/STIs in gay bathhouse attendees. Accordingly, comprehensive prevention efforts need to be incorporated into bathhouse environments, such as the provision of condoms and lubricants, the distribution of HIV/STI information brochures, or the offering of on-site HIV/STIs screening services. These intervention measures can be expected to create an environment for safer sex and to reduce HIV/STIs transmission among male bathhouse attendees.
In summary, men attending gay bathhouses often engaged in unsafe sex practices and were at substantial risk of acquisition of HIV/STI. Irregular use of condoms during oral sex, condom inaccessibility at bathhouses, unprotected sex at public venues, no prior HIV test, and 5 or more visits to bathhouses every month were independently associated with unprotected anal intercourse. The frequent engagement in unprotected sex among bathhouses attendees highlights the potential of acquisition of HIV/STIs and the urgency for preventive campaigns targeting gay bathhouses to be initiated to reduce the frequency of risky sexual behaviors.
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