Lymphogranuloma venereum (LGV) has reestablished itself as an important sexually transmitted infection (STI) among men who have sex with men (MSM) in large US and European cities.1 Several rectal LGV cases have also been reported in Australia.2–5 In common with most reports worldwide, these cases predominantly comprised HIV-infected MSM with symptoms of proctitis attending clinical services.
Previous investigations in North America and the United Kingdom failed to identify a substantial reservoir of subclinical LGV infection among MSM.6–8 However, these studies were predominantly in clinic-based samples. To our knowledge, there are no published estimates of the prevalence of LGV among MSM in the community. To investigate whether there is an asymptomatic pool of LGV in the community, we performed LGV typing on all Chlamydia trachomatis Deoxyribonucleic acid (DNA)-positive specimens identified in 2 community-based cohort studies of HIV-infected and -uninfected MSM in Sydney, Australia.
The methods of the Health in Men (HIM) HIV-uninfected cohort and the Positive Health (pH) HIV-infected cohort studies have previously been published.9 Ethics approval was obtained from the University of New South Wales. In each study, the men underwent annual face-to-face interviews in which detailed behavioral and symptom data were sought. Routine questioning of anal symptoms included recent and current presence of discharge, itch, sores, bleeding, tearing, and pain on defecation.
Comprehensive STI screening was offered annually to participants in both cohorts.9 In consenting participants, C. trachomatis and N. gonorrhoeae testing of urine, pharyngeal swabs, and self-collected anal swabs was performed by strand displacement amplification (SDA) (BD ProbeTec, BD Diagnostics, Sparks, MD, USA). Serovar analysis was performed on all pharyngeal and anogenital samples positive for C. trachomatis DNA from January 2005 until study completion in mid-2007. Serovar analysis of C. trachomatis involved DNA sequencing across all 4 variable domains of the ompA gene encoding for the immunodominant major outer membrane protein, as described previously.10
In the HIV-uninfected and HIV-infected cohort, a total of 2082 (90.2% of eligible visits) and 521 (70.8% of eligible visits) SDA chlamydia tests, respectively, were performed. The total follow-up time was 2005.1 person-years (PY) in the HIV-uninfected cohort and 320.2 PY in the HIV-infected cohort. Participants in both cohorts were predominantly asymptomatic. Any anal symptom was reported by participants at 2.6% (95% CI: 2.2%–3.1%) and 3.7% (95% CI: 2.7%–4.9%) of study visits in the HIV-uninfected and HIV-infected cohorts, respectively.
Among participants in the HIV-uninfected cohort, C. trachomatis was identified on 34 anal (positivity rate, 1.63%; 95% CI: 1.13%–2.27%), 9 urine (positivity rate, 0.43%; 95% CI: 0.20%–0.81%), and 3 pharyngeal (positivity rate, 0.14%, 95% CI: 0.003%–0.42%) samples. Serovar analysis revealed no LGV among these 46 positive chlamydia samples. Among participants in the HIV-infected cohort, chlamydia infection was identified on 13 anal (positivity rate, 2.50%; 95% CI: 1.34%–4.22%), 3 urine (positivity rate, 0.58%; 95% CI: 0.12%–1.67%), and 2 pharyngeal (positivity rate, 0.38%; 95% CI: 0.05%–1.38%) samples. All positive C. trachomatis samples detected on the SDA assay were also positive for chlamydia DNA on the ompA assay. Only 1 of 18 HIV-infected participants diagnosed with C. trachomatis was infected with an LGV serovar (LGV incidence in the HIV-infected cohort 0.3 per 100 PY, 95% CI: 0.008–1.7). The sample, collected in 2005, was an anal swab identified as L2b positive. The LGV-infected participant was 44 years old, reported receptive unprotected anal intercourse with other HIV-infected men in the previous 6 months, and reported mild anal “tearing” on the day of the interview. As per study protocol, the LGV-infected participant was referred to his usual doctor for treatment. Data were not sought in either cohort regarding treatment regimens prescribed by participants' doctors. Nonetheless, anal screening performed the following year as part of the pH study was negative for C. trachomatis.
The majority of participants from both cohorts were recruited at gay community events, and less than 4% were from clinics. Therefore, we believe participants to be broadly representative of gay-community–attached MSM in Sydney.
Outside Australia, LGV appears to be most common in a well-defined sexually adventurous subpopulation of HIV-infected MSM.1 If a representative sample of such men had not been recruited into our cohorts, it is possible that we might have underestimated the prevalence of LGV in the Sydney gay community. Another possible limitation of our analysis is that serovar analysis was only performed on swabs initially testing positive for C. trachomatis on the SDA test. This assay may be less sensitive than other nucleic acid amplification tests for anorectal C. trachomatis detection among MSM.11 Our previous analysis from the HIV negative HIM cohort found pharyngeal chlamydia to be rare in MSM.12 However, nucleic acid amplification tests have not been validated for diagnosis of chlamydia in the pharynx. Thus, some anal and pharyngeal chlamydia infections may have initially been missed and therefore not referred for serovar analysis.
HIV-infected MSM are disproportionately affected by a range of STIs9 including LGV.13 However, we detected relatively few chlamydia infections in our community-based HIV-infected cohort. This may be attributed to frequent STI screening, detection, and treatment performed by their HIV physicians during regular visits for routine HIV care, as has been recommended for Australian HIV-infected MSM.9
Dutch investigators13 have reported a high proportion of asymptomatic anorectal LGV, which contrasts sharply with reports from Australia2–5 and other settings.6,8 No history of recent overseas travel was sought from study participants in either cohort. It is possible that asymptomatic LGV may be detected more frequently in such high LGV prevalence settings as a result of screening MSM during the “presymptomatic” phase.1 Nonetheless, the lack of LGV identified among predominantly asymptomatic MSM in a setting in which clinical cases of LGV have been described2,5 suggests that most LGV in Australian MSM is symptomatic.
To confirm this hypothesis, further community-based studies are required in settings in which clinical LGV is more common among MSM. Our findings concur with those among large clinical samples of MSM6 and suggest that routine LGV typing of chlamydia infections in asymptomatic Australian MSM is not justified at this stage.
1. White JA. Manifestations and management of lymphogranuloma venereum. Curr Opin Infect Dis 2009; 22:57–66.
2. Stark D, van Hal S, Hillman R, et al. Lymphogranuloma venereum in Australia: Anorectal Chlamydia trachomatis
serovar L2b in men who have sex with men. J Clin Microbiol 2007; 45:1029–1031.
3. Morton AN, Fairley CK, Zaia AM, et al. Anorectal lymphogranuloma venereum in a Melbourne man. Sex Health 2006; 3:189–190.
4. Lee DM, Fairley CK, Owen L, et al. Lymphogranuloma venereum becomes an established infection among men who have sex with men in Melbourne. Aust N Z J Public Health 2009; 33:94.
5. van Hal SJ, Hillman R, Stark DJ, et al. Lymphogranuloma venereum: An emerging anorectal disease in Australia. Med J Aust 2007; 187:309–310.
6. Ward H, Alexander S, Carder C, et al. The prevalence of Lymphogranuloma venereum (LGV) infection in men who have sex with men: Results of a multi-centre case finding study. Sex Transm Infect 2009; 85:173–175.
7. Geisler WM, Morrison SG, Bachmann LH. Absence of lymphogranuloma venereum strains among rectal Chlamydia trachomatis
outer membrane protein A genotypes infecting women and men who have sex with men in Birmingham, Alabama. Sex Transm Dis 2008; 35:856–858.
8. Tinmouth J, Gilmour MW, Kovacs C, et al. Is there a reservoir of sub-clinical lymphogranuloma venereum and non-LGV Chlamydia trachomatis
infection in men who have sex with men? Int J STD AIDS 2008; 19:805–809.
9. Jin F, Prestage GP, Zablotska I, et al. High rates of sexually transmitted infections in HIV positive homosexual men: Data from two community based cohorts. Sex Transm Infect 2007; 83:397–399.
10. Stevens MP, Twin J, Fairley CK, et al. Development and evaluation of an ompA qPCR assay for Chlamydia trachomatis
serovar determination. J Clin Microbiol 2010;45:2060–2065.
11. Moncada J, Schachter J, Liska S, et al. Evaluation of self-collected glans and rectal swabs from men who have sex with men for detection of Chlamydia trachomatis
and Neisseria gonorrhoeae
by use of nucleic acid amplification tests. J Clin Microbiol 2009; 47:1657–1662.
12. Templeton DJ, Jin F, Imrie J, et al. Prevalence, incidence and risk factors for pharyngeal chlamydia in the community based Health in Men (HIM) cohort of homosexual men in Sydney, Australia. Sex Transm Infect 2008; 84:361–363.
13. Van der Bij AK, Spaargaren J, Morré SA, et al. Diagnostic and clinical implications of anorectal lymphogranuloma venereum in men who have sex with men: A retrospective case-control study. Clin Infect Dis 2006; 42:186–194.