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Abstract
Objectives Current strategies for controlling non-urogenital chlamydia and gonorrhoea are not uniform. It is assumed that present anorectal/oropharyngeal infections are coincidentally treated with urogenital infections. However, it is not clear whether this control strategy is effective. To inform current debate, we evaluated the anatomical site distribution of chlamydia and gonorrhoea by routine testing in men who have sex with men (hereafter men) and in high-risk women (prostitutes and swingers, hereafter women).
Methods Between January 2010 and November 2012, all men (n=2436) and women (n=1321) attending our sexually transmitted infection clinic were routinely tested for anorectal, oropharyngeal and urogenital Chlamydia trachomatis and Neisseria gonorrhoeae. Data were collected on demographics and sexual behaviour.
Results Overall chlamydia positivity was 10.4% (254/2436) in men and 7.0% (92/1321) in women, for gonorrhoea this was 6.3% (154/2436) and 3.1% (41/1321), respectively. Isolated non-urogenital infections amounted to 76% of all infections in men and for up to 59% of all infections in women. For combined urogenital and anorectal infections, this amounted to 14% for men and up to 54% for women.
Conclusions Testing only for non-urogenital infections is insufficient, as it overlooks many infections. The use of coincidental treatment is therefore a suboptimal control strategy in high-risk groups for halting complications and transmission. There is an urgent need to optimise the testing guidelines for chlamydia and gonorrhoea at different anatomical sites.
- CHLAMYDIA TRACHOMATIS
- NEISSERIA GONORRHOEA
- TESTING
- EPIDEMIOLOGY (GENERAL)
- PUBLIC HEALTH
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Introduction
Anorectal and oropharyngeal chlamydia and gonorrhoea are common in men who have sex with men (1–24%)1–4 and in high-risk women (1–15%).2 ,3 ,5 ,6 Insight into the anatomical site distribution of sexually transmitted infections (STIs) is important to understanding the appropriateness of current strategies for diagnosing and treating anorectal and oropharyngeal chlamydia and gonorrhoea, in order to halt complications and transmission. One common strategy includes coincidental concurrent treatment based solely on the identification of urogenital chlamydia and gonorrhoea, given that few STI clinics2 and even fewer general practitioners (0.1%)7 routinely test for non-urogenital chlamydia and gonorrhoea. This strategy can be effective only if (1) non-urogenital infections occur mainly in the presence of urogenital infections and (2) the same treatment regimen is appropriate for the different anatomical sites. Previous studies have demonstrated that symptom-based testing is not an effective strategy, but history based testing may be and these studies seem to have informed much of current practice.1 ,2 ,4–6 Studies on symptom-based and sexual history-based testing (selective testing) have revealed high shares of combined urogenital and anorectal infections (chlamydia 63–90%, gonorrhoea 56–73%) in high-risk women attending STI clinics.2 ,3 ,5 ,6 and high shares of isolated anorectal chlamydia (54–91%) and gonorrhoea (21%)1 ,2 ,4 for all diagnosed infections in men who have sex with men. Up till now, only three studies have applied routine universal testing that is, not based on symptoms or sexual history. One study examined the sensitivity of symptom-based and sexual history-based testing for anorectal STI: sensitivity was low (40–52%) and this procedure is likely to miss a substantial number of anorectal infections.3 Two studies examined oropharyngeal STI in men who have sex with men and reported substantial shares of isolated oropharyngeal chlamydia (68%) and gonorrhoea (98%).8 ,9 Moreover, the appropriate treatment for anorectal chlamydia is the subject of ongoing debate. Several studies have reported substantial microbial failure rates of up to 21% for single-dose azithromycin (1.0 g) in anorectal chlamydia.10 Guidelines from the Netherlands and the UK currently advocate 7 days of doxycycline 100 mg twice daily as a first-line treatment, and azithromycin is advocated as equal treatment by the US Centers for Disease Control.
To inform the current debate on appropriate strategies for controlling anorectal and oropharyngeal infections, we evaluated the anatomical site distribution of chlamydia and gonorrhoea by performing routine universal testing at urogenital, anorectal and oropharyngeal site in men who have sex with men and in high-risk women.
Methods
From January 2010 to November 2012, all men who have sex with men and all high-risk women aged 18 years or older who attended the South Limburg Public Health Service's STI clinic were routinely tested for urogenital, anorectal and oropharyngeal Chlamydia trachomatis and Neisseria gonorrhoeae. In total, 17% (n=776) of patient population was not tested at all anatomical sites. Coverage varied by risk group and time; 88–95% in men who have sex with men, 91–95% in swingers and 25–46% in prostitutes. A total of 2436 consultations by 1218 men and 1321 consultations by 516 women were used for analyses. Men who have sex with men (hereafter men) were defined as men who had engaged in sex with one or more men in the past 6 months. High-risk women (hereafter women) included prostitutes and swingers.3 Swingers were defined as women who were part of a male-female couple who as a couple had sex with other male-female couples and their self-identified heterosexual sex partners. Prostitutes were defined as women who reported to have had sex for money in the past 6 months. Of the 1321 women, 18.7% were prostitute (n=247) and 81.3% were swinger (n=1074). At our STI clinic there is no current test of cure practice and individuals are not retested within 3 months. The median number of days between repeat tests was 171 (IQR 105–228). The specimens tested consisted of self-collected vaginal swabs or urine, anorectal swabs and clinician-collected oropharyngeal swabs.3 Specimens were processed at two regional laboratories using three different nucleic acid amplification assays (NAATs) (SDA, Becton Dickinson ProbeTec ET system, Maryland, USA and PCR, Cobas Amplicor, Roche, California, USA and PCR, Cobas 4800, Roche, California, USA). Serum was tested for Treponema pallidum haemagglutination and HIV.
Statistical analysis
Variables were constructed according to the following mutually exclusive categories: isolated anorectal (including combined anorectal, oropharyngeal infection), combined urogenital and anorectal (including combined urogenital, anorectal and oropharyngeal infection), isolated oropharyngeal and isolated urogenital infection (including combined urogenital, oropharyngeal infection). χ2 tests were used to compare the distribution of infections across the various anatomical sites, as well as across demographic and behavioural factors for men and women. Analyses were performed using SPSS V.17.0.0 (IBM, Somers, New York, USA). The Medical Ethics Committee of Maastricht University (Identification number 11-4-108) approved the study.
Results
Of the 3757 men and women, the median age was 37 years (IQR: 25–47 years) for men and 43 years (IQR: 36–49 years) for women. The majority (>95%) were Caucasian. Men reported having had a median of four sex partners in the past 6 months (IQR: 2–10), while women reported seven (IQR: 4–13). The prevalence of HIV and syphilis was 12.5% and 15.3%, respectively, for men, and 0% and 0.5%, respectively, for women. The prevalence of chlamydia (ie, a positive result in at least one of three tested anatomical sites) was 10.4% (254/2436) for men and 7.0% (92/1321) for women. For gonorrhoea, the prevalence rates were 6.3% (154/2436) and 3.1% (41/1321), respectively. Chlamydia and gonorrhoea co-infection was present in 1.2% (n=30) of men and 0.2% of women (n=3). Overall, 23–76% of all infections were isolated non-urogenital (table 1).
Prevalence of urogenital, anorectal and oropharyngeal chlamydia and gonorrhoea, and anatomical site distribution of chlamydia and gonorrhoea in men who have sex with men and in high-risk women by routine anorectal, urogenital and oropharyngeal testing
Discussion
This is the first study to provide a systematic assessment of the anatomical site distribution of chlamydia and gonorrhoea with routine universal urogenital, anorectal and oropharyngeal testing in men and in women. The proportion of isolated non-urogenital infections among all chlamydia and gonorrhoea infections was substantial for men (up to 76%) and women (up to 59%). Urogenital testing alone is thus not an appropriate diagnostic strategy for detecting anorectal and oropharyngeal chlamydia and gonorrhoea in these high-risk groups. Treatment of urogenital infections alone overlooks many infections in high-risk groups such as studied here, and it therefore excludes many patients from proper treatment. The high proportion of isolated oropharyngeal gonorrhoea in women is notable. The relative importance of these oropharyngeal infections in the burden of disease (whether clinical or otherwise) is unclear, as is their share in transmission and the speed with which they can be cleared. In a previous study, we showed that the sensitivity of anorectal testing based on behavioural indications or symptoms is low.3 Combined urogenital and anorectal chlamydia occurred in 14% of men and in 54% of women. Our results are consistent with previous reports that demonstrate high shares of isolated infections in men and high shares of combined infections in women.1 ,2 ,4–6 It is not known whether concurrent treatment with azithromycin would constitute sufficient treatment for such combined infections. Some evidence suggests that azithromycin is suboptimal in treating anorectal chlamydia.10 Our study sample did not include unique individuals only, which may be a limitation. However, restricting to first consultations in analysis gave similar results, therefore we expect bias to be minimal. Sensitivity and specificity of NAATs are high, although not 100%. False positives may occur in lower-prevalence populations for example in the case of low prevalence of oropharyngeal STI. Furthermore, we could not completely rule out the possibility of autoinoculation by infected vaginal secretions in women. However, regardless of transmission route, anorectal infections can cause further STI transmission. Although our instructions on specimen collection were clear, we cannot entirely rule out the possibility of specimen contamination, for example, via the urogenital-anorectal route. Prostitutes had relatively low coverage. However, this group comprised a small part (19%) of women and the anatomical site distributions of prostitutes and swingers were similar (data not shown). This may indicate that possible bias due to incomplete testing in prostitutes is minimal. However, it also warrants more research in prostitutes. The results of this study suggest routine universal testing could be preferable for high-risk clients of STI clinics. Although we cannot extrapolate these results to other populations and care settings, our study demonstrates the need for further research in diverse settings to determine the need for multiple anatomical site testing.
Acknowledgments
The authors acknowledge the contributions of the staff of the STI clinic, South Limburg in collecting the data.
Footnotes
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Handling editor Khalil Ghanem
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Contributors CJPAH and NHTMD-M were involved in the conception and design of the study. GAFSvL produced the database, analysed the data and wrote the first draft of the manuscript. All of the authors contributed to writing the paper; all had full access to all of the data in the study, and all can take responsibility for the integrity of the data and the accuracy of the data analysis.
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Funding This study was supported by the Centre for Infectious Disease Control, the National Institute for Public Health and the Environment (RIVM) (project number: V/215602/01/SO).
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Competing interests All authors have completed the ICMJE uniform disclosure form at http://www.icmje.org/coi_disclosure.pdf (available upon request from the corresponding author) and declare the following: no support from any organisation for the submitted work; no financial relationships with any organisations that might have an interest in the submitted work in the previous 3 years; no other relationships or activities that could appear to have influenced the submitted work.
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Patient consent Obtained.
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Ethics approval The Medical Ethics Committee of Maastricht University.
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Provenance and peer review Not commissioned; externally peer reviewed.