Lister, N. A. BA/Sc(Hons)*; Smith, A. BSc(Hons), PhD†; Tabrizi, S. PhD‡; Hayes, P. RN, BApSc§; Medland, N. A. MBBS∥; Garland, S. MD, FRCPA‡; Fairley, C. K. PhD, FRACP§
*Department of Public Health, The University of Melbourne, Melbourne, Australia; the †Australian Research Centre in Sex, Health and Society, La Trobe University, Melbourne, Australia; the ‡Department of Microbiology & Infectious Diseases, Royal Women's Hospital, Women's and Children's Health, Carlton, Australia; §Melbourne Sexual Health Centre, Melbourne, Australia; and ∥The Centre Clinic, Victorian AIDS Council, Gay Men's Health Centre, South Yarra, Australia
The authors thank the staff of the Molecular Microbiology unit at the Royal Women's Hospital in Melbourne who performed the PCR testing of all specimens (Gemma Eldridge, Shujun Chen, and Elice Rudland); the proprietors and staff members of the 6 participating venues; and the nursing staff of the Melbourne Sexual Health Centre for recruiting participants, liaison with venue staff, and input in the development of a recruitment strategy (Tom Carter, Peter Hayes, David Lee, Steven Hill, and Phillip Patterson).
A/Prof. Smith is supported by a Senior Research Fellowship from the Victorian Health Promotion Foundation, and funding for this study was provided by the Victorian Department of Human Services.
Correspondence: N. A. Lister, BA/SC(Hons), The University of Melbourne, School of Population Health, Sexual Health Unit, Melbourne Sexual Health Centre, 580 Swanston Street, Carlton 3053, Victoria, Australia. E-mail: firstname.lastname@example.org
Received for publication March 18, 2003,
revised July 21, 2003, and accepted July 22, 2003.
OVER THE LAST 5 YEARS, a number of industrialized countries have reported increases in sexually transmissible infections (STIs) and risk behaviors for STI and HIV transmission among men who have sex with men (MSM). 1–5 Many reports of these increases have focused on STI rates and the implications for control of STI-associated HIV infection. To reduce STI-associated HIV transmission, a number of international bodies have recommended screening programs for MSM to detect the substantial proportion of infections that are asymptomatic.
Guidelines for screening programs have been developed for several industrialized countries, including Australia. 6–9 These guidelines target MSM attending sexual health clinics and general medical practices, but could fail to reach MSM not attending clinical services. To overcome this, some public health programs in Australia have targeted MSM attending male-only saunas. 10–12 Anecdotal reports and case reviews have suggested STI acquisition could be linked with anonymous sex partners in male-only saunas (unpublished observations). 2,13 We conducted a cross-sectional study of MSM attending local male-only saunas to determine 1) the participation rate of STI screening during a visit at a sauna, and the proportion who would follow up their test results; 2) the prevalence of selected STIs; and 3) to evaluate risk factors for STI acquisition. Gonorrhea and chlamydia screening was offered to men, and it was anticipated that this study would function as a pilot to investigate the feasibility of implementing a comprehensive STI screening service, including HIV testing.
Study Design and Sampling
This was a cross-sectional study conducted in 6 male-only saunas in Melbourne, Australia. Each sauna was visited regularly for a minimum of 8 weeks between October 2001 and September 2002 (mean number of hours per visit, 3.2; total number of hours of recruitment, 153).
Male nurses trained in sexual health approached sauna patrons and invited them to participate in the program. Patrons were only approached if they were 1) standing or sitting alone, 2) in an area with good lighting, and 3) in areas thought to be unlikely sites for sexual activity, eg, near the locker rooms or reception. A key consideration was the personal safety of nurses and not wanting to be intrusive of patrons’ activities in the saunas.
Promotion of the study at the saunas was minimal and only occurred during periods when the nurses were recruiting. A poster was positioned at each sauna in an area where potential participants were approached. The poster displayed simple text messages to inform men that they might be approached and offered testing during their visit at the sauna.
Patrons who agreed to participate were screened for gonorrhea and chlamydia, and self-completed a short questionnaire. Because HIV testing was not offered, participants were briefly counseled about sexual health, including HIV testing, and given referrals if necessary. Participants were not paid or offered incentives, but the service was free. All participants were given written information about the project and consent was obtained verbally. Patrons who declined to participate were only encouraged to offer explanation for why they did not want to participate. Collection of demographic or other information was not possible without consent, and excluding them allowed the nurse to spend time approaching other patrons. The project was approved by the Victorian Department of Human Services Human Research Ethics Committee.
No identifying information was obtained from participants. Each participant was given a card with a unique study number and an 1800 (free call) telephone number to obtain their results. This number was answered between 9 am and 5 pm Monday through Friday. Participants testing positive were referred to the Melbourne Sexual Health Center or a preferred general practitioner.
Each participant was given a 1-page questionnaire. The questionnaire asked about participant demographics (age); the presence of a sore throat, urethral, or rectal symptoms in the previous week; the number of male and female sexual partners in the previous month; the practice of unprotected oral and anal intercourse in the previous month; and the number of visits to beats, male-only saunas, and sex clubs that resulted in sex (any).
Specimen Collection and Transport
Participants collected a first-pass urine sample and inserted a sterile swab 2 to 4 cm into their anus. Nurses collected the throat swabs. The specimens were refrigerated and transported at 4°C to the Molecular Microbiology Laboratory of the Royal Women's Hospital in Melbourne, Australia, for nucleic acid amplification testing (NAAT). Specimens were tested within 96 hours of receipt.
Urine samples were processed and tested for Chlamydia trachomatis and Neisseria gonorrhoeae by polymerase chain reaction (PCR) using COBAS AMPLICOR assay (Roche Molecular Diagnostics, Branchburg, NJ) as per the manufacturer's instructions. The testing also included an internal coamplified control target. Samples negative for the internal control were confirmed by repeat testing and those negative on 2 occasions were designated as unassessable.
Throat and anal swabs were each rotated in 200 μL of phosphate-buffered saline (PBS), and resulting cell suspensions were extracted using the automated MagNA Pure LC (Roche Diagnostics) with the associated DNA Isolation Kit I protocol. DNA was eluted in a final volume of 100 μL of MagNA Pure Elution Buffer (Roche Diagnostics).
Aliquots of 12.5 μL of each extracted DNA from throat and anal sites from each patient were pooled and tested for C. trachomatis by mixing with 25 μL of Specimen Diluent followed by 10-minute room temperature incubation before amplification using Roche COBAS AMPLICOR. 14 Positive samples for C. trachomatis were retested using nonpooled DNA to determine the site from which the sample was positive.
Extracted DNA from throat and anal sites were tested for N. gonorrhoeae using primers and probes directed at a 273 base pair region of cpp gene located on a 4.3-kb cryptic plasmid as previously reported 14 with modification of adaptation of assays to real-time assay on LightCycler (Roche Diagnostics). All urine N. gonorrhoeae- positive samples were also confirmed by this method. β-globin amplification was included as a positive internal control, which is directed to amplify a human β-globin product of 260 bp. 15
Strict procedures avoiding specimen contamination and carryover were followed.
Data analyses were conducted using the SPSS 11.0 for Windows software (SPSS, Chicago, IL). Data in categories were evaluated using χ2 or Fisher exact test analyses; comparisons of continuous data were conducted with t tests or analysis of variance. Confidence intervals for proportions were determined using the binomial distribution.
Of 2140 men approached, 521 (24%) agreed to participate in the study. The reasons for declining to participate were a recent STI check-up (17%), preferred general practitioner (17%), had no self-perceived sexual risk or symptoms (13%), or concern about confidentiality (1%). The majority of men gave no reason (45%) and did not want to talk further with the nurse on duty. No demographic or sexual health data were collected on those who declined to participate.
The proportion of participants with PCR-detected gonorrhea and/or chlamydia infection was 10.7% (95% confidence interval [CI], 8.1–13.4%). Among the 6 different venues, the detection of any infection ranged between 7.7% and 18.6% (P = 0.45). The mean age of all participants was 40.1 years (standard deviation, 12.1); and among the 6 venues, the mean age was significantly different (P <0.001).
Of the 521 participants, 511 collected a urine sample. Chlamydia was detected in 9 samples (1.8%; 95% CI, 0.8–3.3%). Gonorrhea was detected in 1 sample (0.2%; 95% CI, 0–1%), which was also chlamydia-positive. Urethral symptoms were reported by 2 of 9 participants with urethral infection (22%) and 23 of 498 participants without urethral infection (4.6%) (P = 0.016). Of the 25 participants reporting urethral symptoms, 6 had sought treatment from their usual doctor and 14 reported having not sought treatment.
Of the 521 participants, 507 collected a rectal swab. Chlamydia was detected in 30 rectal swabs (5.9%; 95% CI, 4–8%), and gonorrhea was detected in 11 swabs (2.2%; 95% CI, 1–4%), including 4 rectal samples positive for both pathogens. Anorectal symptoms were reported by 5 participants with chlamydia-positive rectal swabs and 2 participants with gonorrhea-positive rectal swabs. Overall, anorectal symptoms were reported by 7 of 36 participants with rectal infection (19.4%) and 39 of 427 participants without rectal infection (8.1%) (P = 0.026). Of the 46 participants reporting anorectal symptoms, 9 had sought treatment from their usual doctor, t2wo saw a new doctor, and 28 reported having not sought treatment.
Throat swabs were collected from all 521 participants. Chlamydia was detected in 3 throat swabs (0.6%; 95% CI, 0.1–1.7%), and gonorrhea was detected in 13 swabs (2.5%; 95% CI, 1.3–4.2). A sore throat was reported by 4 of 16 participants with throat infection (25%) and 115 of 504 participants without throat infection (22.8%) (P = 0.838). Of the 119 participants reporting a sore throat, 23 had sought treatment from their usual doctor, and 83 reported having not sought treatment.
Overall, of 56 men testing positive for gonorrhea and/or chlamydia infection, 13 (23.2%) reported site-specific symptoms.
The internal control was negative (a marker of inhibition for PCR in the sample) in 2 urine samples (0.4%), 20 rectal swabs (3.9%), and 7 throat swabs for chlamydia detection (1.3%), and in 2 urine samples (0.4%), 16 rectal swabs (3.2%), and 5 throat swabs for gonorrhea detection (1.0%).
The presence of any infection was statistically associated with a younger age and seeking sexual health care in the last year, but not other factors (Table 1). The presence of infection with gonorrhea was statistically associated with a younger age and seeking sexual health care in the last year, and any unprotected anal intercourse in the previous month, but not other factors. The presence of infection with chlamydia was only statistically associated with younger age groups. Multivariate analyses revealed that only seeking sexual health care in the last year remained a significant predictor of infection; other factors did not (data not shown).
A total count of 365 (70%) participants obtained their test results. This was not different between those with and without infection (P = 0.7), ie, 30% of those testing positive did not obtain their test results. Of the participants who have obtained their test results, 337 (92%) telephoned the designated 1-800 line, 19 (5%) returned to a sauna and obtained results from an outreach nurse, 7 (2%) through e-mail, and 2 (1%) contacted the Melbourne Sexual Health Center directly.
Our study showed that men approached for STI testing at male-only saunas had a high prevalence rate of gonorrhea and chlamydia that was largely asymptomatic. Rectal infection was most common for both gonorrhea and chlamydia. Pharyngeal infection with chlamydia and urethral infection with gonorrhea were rare. In general, behavior over the last month did not predict the presence of an infection, suggesting infections could have been present for sometime. The exception to this was unprotected anal intercourse and gonorrhea. These findings support the implementation of a comprehensive screening service, including HIV testing, in Melbourne saunas.
Surprisingly, participants recently seeking care or treatment for their sexual health had a higher risk of infection. This finding suggests that frequent contact with healthcare providers could be a marker of high risk for STI acquisition. An alternative explanation is that the visit to their healthcare provider did not involve testing for infection at all the recommended sites. We did not collect information about testing done during recent visits to healthcare providers.
Possible explanations as to why behavior over the last month did not predict infection include 1) participants underreporting high-risk sexual behavior, or 2) only recording sexual history data from the previous month. It is unlikely that underreporting of certain behaviors explains this finding because the confidentiality and anonymity of participation is more likely to encourage the veracity of responses. It is possible that a substantial number of infections were acquired more than 1 month ago and, therefore, recent behavior was not an accurate predictor of the infections.
This study used NAAT assays for detection of gonorrhea and chlamydia. In published literature, there are few reports of evaluation of NAATs for rectal and pharyngeal, and, in fact, these samples are not validated by most commercial assays. However, the assay protocol described in this study has a number of additional steps to allow for confident testing of rectal and pharyngeal samples, for example, extraction of DNA before testing, testing for adequacy of samples by β-globin amplification, and confirmation of N. gonorrhoeae-positive samples by a supplementary PCR assay (with a different target). These additional steps facilitate specificity and the reduction of inhibitors. 14 In addition, all chlamydia-positive samples were confirmed by PCR amplification of the omp1 gene and subsequent sequencing, and a number of gonorrhea-positive samples were confirmed by sequencing of the probe binding region of the cpp gene (data not shown). For these reasons, it is unlikely that the NAATs used for this study have contributed to the lack of association between recent behavior and infection.
The findings of our study have highlighted the importance of STI/HIV prevention programs targeting MSM in male-only saunas. Future screening programs in Melbourne saunas should seek to improve on the low participation rate (24%) and to increase the proportion obtaining test results (70%). It is possible that participants were limited by the 1800 (free call) line that was only available between 9 am and 5 pm Monday through Friday for collection of test results. Also, future programs should attempt to obtain contact details for follow up of positive test results. A number of different approaches might need to be used simultaneously to encourage participation and to increase nurse contact with sauna patrons. For example, greater promotion of the service by advertising or handing out information cards at the sauna, or offering incentives to participate such as free entry to the sauna. Finding a balance between making screening available and limiting the intrusiveness on sauna patrons will be important to the success of future programs. Also, working with sauna proprietors and staff and improving the service based on client feedback will be important for these key stakeholders to take ownership of future programs.
Although we have not determined the prevalence of HIV infection among Melbourne sauna patrons, the findings have highlighted the potential for increases in HIV infections among MSM using saunas. For this reason, it can be argued that more focus should be placed on HIV-positive men who use saunas. Future screening programs in saunas need to include HIV testing and appropriate counseling, and all men using saunas should be encouraged to participate in regular STI screening, regardless of HIV serostatus.
The high prevalence of gonorrhea and chlamydia in Melbourne male-only saunas identified in this study is rationale for continuing with a more comprehensive screening service. However, this study has identified that the uptake of screening opportunities in saunas by patrons could be a problem with future programs. It will be important for a screening program to work with sauna proprietors, sauna staff, and patrons to deliver an acceptable service for all stakeholders. This alongside a comprehensive service and clever promotion could encourage MSM in saunas to take active care for their sexual health.
1. National Centre in HIV Epidemiology, Clinical Research. HIV/AIDS, viral hepatitis and sexually transmissible infections in Australia Annual Surveillance Report 2002. National Centre in HIV Epidemiology and Clinical Research, The University of New South Wales, Sydney, NSW. 2002. Available at: http://www.med.unsw.edu.au/nchecr
2. Anonymous. Resurgent bacterial sexually transmitted disease among men who have sex with men—King County, Washington, 1997–1999. MMWR Morb Mortal Wkly Rep 1999; 48: 773–777.
3. Fox KK, del Rio C, Holmes KK, et al. Gonorrhea in the HIV era: a reversal in trends among men who have sex with men. Am J Public Health 2001; 91: 959–964.
4. Wolitski RJ, Valdiserri RO, Denning PH, et al. Are we headed for a resurgence of the HIV epidemic among men who have sex with men? Am J Public Health 2001; 91: 883–888.
5. Handsfield H. Conference Report. Highlights from the 2002 STD Conference. In: National STD Prevention Conference; May 2002; San Diego, California; Medscape Portals Inc, Medscape Infectious Diseases 2002; 4(1). Available at: http://www.medscape.com
6. Public Health—Seattle, King County. Sexually transmitted diseases and human immunodeficiency virus screening guidelines for men who have sex with men. Sex Transm Dis 2001; 28: 457–459.
8. California Sexually Transmitted Disease Controllers Association (STDCA), California Coalition of Local AD. Guidance for STD clinical preventive services for persons infected with HIV. Sex Transm Dis 2001; 28: 460–463.
9. Australian College of Sexual Health Physicians. Draft October 2002 Clinical Guidelines for the Management of Sexually Transmissible Infections among Priority Populations. Available at: http://www.ashm.org.au
. Accessed October 2002.
10. Dunne MP, McCamish M, Hamilton K. HIV testing of homosexual and bisexual men. Med J Aust 1992; 157: 212.
11. Debattista J, Dwyer J, Orth D, et al. Community screening for Neisseria gonorrhoeae
and Chlamydia trachomatis
among patrons of sex-on-premises venues: two years later. Venereology 2000; 13: 105–109.
12. Debattista J, Clementson C, Mason D, et al. Screening for Neisseria gonorr
hoeae and Chlamydia trachomatis
at entertainment venues among men who have sex with men. Sex Transm Dis 2002; 29: 216–221.
13. Binson D, Woods WJ, Pollack L, et al. Differential HIV risk in bathhouses and public cruising areas. Am J Public Health 2001; 91: 1482–1486.
14. Tabrizi SN, Fairley CK, Cehn S, et al. Evaluation of patient-administered tampon specimens for Chlamydia trachomatis
and Neisseria gonorrhoeae
. Sex Transm Dis 2000; 27: 133–137.
15. Resnick RM, Cornelissen MT, Wright DK, et al. Detection and typing of human papillomavirus in archival cervical cancer specimens by DNA amplification with consensus primers. J Natl Cancer Inst 1990; 82: 1477–1484.