Objectives: To determine the prevalence, incidence and risk factors for pharyngeal Chlamydia trachomatis in the community based Health in Men (HIM) cohort of HIV negative homosexual men in Sydney, Australia.
Methods: From January 2003, all HIM participants were offered annual screening for pharyngeal chlamydia using BD ProbeTec nucleic acid amplification testing (NAAT). Detailed sexual behavioural data were collected every 6 months, and risk factors for infection and hazard ratios were calculated using Cox regression.
Results: Among 1427 participants enrolled, the prevalence of pharyngeal chlamydia on initial testing was 1.06% and the incidence rate was 0.58 per 100 person-years. More than 50% of all infections were identified on baseline testing and 68% of men with pharyngeal infection had no evidence of concurrent anogenital chlamydia. There was no association of pharyngeal chlamydia with sore throat. Infection was significantly associated with increasing frequency of receptive penile–oral sex with ejaculation with casual partners (p = 0.009), although approximately half of infections occurred in participants not reporting this risk behaviour. Neither kissing nor oro-anal practices were associated with infection.
Conclusion: The incidence of pharyngeal chlamydia infection in the HIM study was relatively low; however, the relatively high prevalence on baseline testing compared to incidence suggests a long duration of infection. Occasional screening for pharyngeal chlamydia in homosexual men who frequently practise receptive oral sex with ejaculation may be warranted.
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In 1977, the first case report was published describing culture isolation of Chlamydia trachomatis from the pharynx of a homosexual man.1 Since then, the prevalence of pharyngeal chlamydia identified among men who have sex with men (MSM) attending clinics has been around 1%,2 3 irrespective of the diagnostic method used. Despite infrequent identification of C trachomatis in the pharynx of MSM, a recent survey found that one-quarter of UK genitourinary medicine clinics offer routine pharyngeal chlamydia screening to MSM attendees.4 As no prospective data exist, we sought to investigate prevalence, incidence and predictors of pharyngeal C trachomatis among the community based Health in Men (HIM) cohort of homosexual men in Sydney, Australia.
Participants were HIV negative men who were recruited mainly from community based sources between June 2001 and December 2004, and followed until June 2007. The methods of the HIM study have been described elsewhere.5 6
Participants underwent annual face-to-face interviews, including detailed sexual behaviours and pharyngeal symptoms. Data on sexual behaviour were also collected at 6 monthly telephone interviews between these visits.
Nucleic acid amplification tests (NAAT) for C trachomatis and Neisseria gonorrhoeae were introduced to the HIM study in January 2003. The HIM study nurse performed a pharyngeal swab on consenting participants by wiping the tonsils, tonsillar crypts and posterior pharynx at the time of the annual face-to-face interviews. Swabs were tested using the BD ProbeTec assay (BD Diagnostics, Sparks, MD, USA) as per the manufacturer’s instructions. Men who tested positive were referred to their usual doctor for treatment, usually with a single oral dose of 1 g azithromycin.
Since NAAT testing was added to the study in January 2003, incidence calculation was only applicable from 2003 forward. In order to incorporate baseline data for incidence analyses, one person-year was allocated for participants’ initial tests as previously described.6
Statistical analyses were performed using STATA 10.0 (STATA Corporation, College Station, TX, USA). For the calculation of incidence, the date of infection was assumed to be the midpoint between the face-to-face interview when participants were diagnosed with pharyngeal chlamydia and the last face-to-face interview. For cases that were diagnosed at the baseline interview, the date of infection was assumed to be 6 months prior. Predictors of pharyngeal chlamydia were assessed using Cox regression and the association with symptoms was assessed using logistic regression. Standard errors were adjusted for repeated measures in the same individuals. All covariates were tested at the 0.05 level of significance and the multivariate model was developed using forward stepwise techniques.
From June 2001 to December 2004, 1427 participants were enrolled. The median age at enrolment was 35 years (range 18–75 years). Over 95% of participants self identified as gay or homosexual and median follow up time to the end of the HIM study was 3.9 years.
A total of 4090 C trachomatis pharyngeal NAATs (90.2% of eligible visits) were performed during the study period. On initial testing (n = 1227), 13 pharyngeal C trachomatis infections were identified; a prevalence of 1.06% (95% confidence interval (CI) 0.57 to 1.84%). Of a total of 25 infections identified, 17 participants (68%) had chlamydia only in the pharynx. Seven participants (28%) had coexisting anal infection and one had C trachomatis simultaneously detected at genital, anal and pharyngeal sites. No participants were co-infected with both C trachomatis and N gonorrhoeae in the pharynx.
Symptom data were available for 23 of the 25 participants with pharyngeal chlamydia and there was no association of infection with pharyngeal symptoms in the past week. Sore throat was reported at 13.0% of visits in those with chlamydia and 18.1% of visits in those without chlamydia (odds ratio (OR) 0.68, 95% CI 0.20 to 2.29, p = 0.533).
The incidence rate of pharyngeal C trachomatis infection during the study period was 0.58 per 100 person-years (95% CI 0.39 to 0.85). No repeat infections were identified. None of the demographic factors considered, including age, education and income, were associated with pharyngeal chlamydia on univariate analysis (data not shown). Only one participant with pharyngeal chlamydia reported sexual contact with someone known to have chlamydia in the last 6 months.
Pharyngeal chlamydia was only detected in participants who reported casual sexual partners in the last 6 months. Table 1 shows univariate and multivariate analyses of sexual behaviours with casual partners as predictors of pharyngeal chlamydia infection. The only sexual behaviour with casual partners independently associated with incident pharyngeal C trachomatis infection was more frequent receptive penile–oral sex with ejaculation (table 1). Pharyngeal chlamydia was not associated with kissing or oro-anal sexual practices.
The baseline prevalence of pharyngeal C trachomatis infection in this community based cohort of HIV negative homosexual men was 1.06% and incidence was 0.58 per 100 person-years. Pharyngeal chlamydia was independently associated with receptive penile–oral sex with casual partners involving ejaculation.
Similar rates of pharyngeal chlamydia have been identified by others screening high risk MSM in community based settings.7 One recently published cross-sectional study examined risk factors for pharyngeal chlamydia among MSM in a London genitourinary medicine clinic.3 No demographic or behavioural associations of infection were found, but only seven pharyngeal chlamydia infections were identified. However, an association between pharyngeal chlamydia and receptive penile–oral sex has previously been described among heterosexual female sexually transmitted disease clinic attendees.8 It is possible that receptive penile–oral sex without ejaculation is associated with pharyngeal C trachomatis infection. However, this sexual behaviour was nearly universal among HIM participants (table 1) and thus the statistical precision of our estimates of association were limited.
The association of pharyngeal chlamydia with receptive penile–oral sex was identified in our study only in connection with ejaculation. Chlamydia may infect multiple sites in the male reproductive tract other than the urethra9 and thus ejaculation could plausibly increase the risk of C trachomatis transmission to the pharynx during penile–oral sex. Nonetheless, this behaviour was reported by less than half of infected participants (table 1) suggesting that ejaculation, while it may increase the risk, is not necessary for chlamydial transmission to the pharynx.
A couple of limitations should be taken into account when interpreting these results. First, the low incidence of pharyngeal chlamydia infection limited statistical power to detect factors associated with infection. Second, the BD ProbeTec assay has not been widely validated for non-genital specimens. At the pharyngeal site, the uniformly low yield of chlamydia infection in MSM populations has precluded firm conclusions regarding test performance where several diagnostic tests are compared.10 Nonetheless, the BD ProbeTec assay has been reported to have a sensitivity of 86–100% and specificity of 100% in clinic based samples for diagnosis of pharyngeal C trachomatis.3 10
Several facets of pharyngeal chlamydia infection remain to be elucidated. The natural history is poorly understood and it remains to be seen whether, like pharyngeal N gonorrhoeae infection,11 it spontaneously resolves within a matter of weeks. However, the fact that more than half of all infections diagnosed in this study were identified at baseline suggests a long duration of pharyngeal C trachomatis infection in the absence of regular testing and treatment. A similar pattern has been suggested for genital chlamydia infections.12
It is unclear how readily urethral C trachomatis infections are transmitted from the pharynx of an infected individual. Previous work in our cohort has found insertive penile–oral sex and receptive oro-anal sex to be important in the transmission of C trachomatis infections of the urethra and anus, respectively.6 Limited data in MSM attending clinics supports the hypothesis that penile–oral sex accounts for some urethral infections.2 13 Thus it is plausible that a substantial proportion of these infections may have been acquired from the pharynx, and that pharyngeal infection plays a role in maintaining a high prevalence of chlamydial infection in MSM.
These are the first prospective data addressing pharyngeal chlamydia infection in MSM and demonstrate a low incidence of pharyngeal C trachomatis among HIV negative homosexual men in Sydney. In view of the relatively high baseline prevalence and association with penile–oral sex, further research should attempt to define the natural history of chlamydial pharyngeal infection. Should longstanding asymptomatic pharyngeal chlamydia be the source of a substantial proportion of anogenital infections, occasional screening of this site could play a role in reducing anogenital chlamydia prevalence among MSM.
Pharyngeal Chlamydia trachomatis infection was infrequently identified in this first prospective study of pharyngeal chlamydia in homosexual men.
More than half of all pharyngeal chlamydia infections were identified on baseline testing suggesting that C trachomatis infection may persist for long periods in the pharynx in the absence of screening.
Two-thirds of chlamydia infections in the pharynx occurred without concurrent anogenital chlamydia infection.
Receptive penile–oral sex with ejaculation was the only predictor of pharyngeal C trachomatis, although approximately half of infections occurred in participants not reporting this behaviour.
We thank all the participants, the dedicated HIM Study team and the participating doctors and clinics. Thanks are also given for the laboratory support from the Molecular Lab at SydPath, especially to Mr Leon McNally. We thank Becton Dickinson for providing testing materials for gonorrhoea and chlamydia.
Funding: During the study DJT was supported by National Health and Medical Research Council Public Health Scholarship no. 351044 and is currently supported by the Royal Australasian College of Physicians GSK Scholarship for virological research. The National Centre in HIV Epidemiology and Clinical Research and the National Centre in HIV Social Research are funded by the Australian Government Department of Health and Ageing. The Health in Men Cohort study was funded by the National Institutes of Health, a component of the US Department of Health and Human Services (NIH/NIAID/DAIDS: HVDDT Award N01-AI-05395), the Australian Government Department of Health and Ageing (Canberra) and the New South Wales Health Department (Sydney), and the National Health and Medical Research Council (project grant # 400944).
Competing interests: None.
Ethics approval: Granted by the University of New South Wales.
Contributors: DJT performed the analyses and drafted the manuscript; AEG took overall responsibility for the project and assisted in the analyses and drafting of the manuscript; FJ, JI, GPP, BD, PHC, SK and JMK assisted in formulating the analyses and drafting the manuscript.
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