Although it has been known for some time that Chlamydia trachomatis can infect the urethra, rectum and pharynx of men who have sex with men (MSM), the prevalence of chlamydiae among MSM has been generally considered to be low, and few sexual health clinics routinely screen for this infection. Recent studies, however, have shown that significant proportions of MSM attending clinics have urethral or rectal chlamydial infection, as detected by nucleic acid amplification tests (NAAT). For example, Manavi et al1 reported that 7% of 443 MSM who consecutively attended the Edinburgh clinic had rectal chlamydial infection, and Arnot et al2 reported a prevalence of urethral infection of 6% among MSM attending the same clinic. Most studies, however, have shown a low rate (<1%) of pharyngeal chlamydial infection.3 4

Much of the current interest in chlamydial infection among MSM has arisen from the recent outbreaks of lymphogranuloma venereum (LGV) proctitis among MSM in western Europe.5 6 In the United Kingdom, more than 400 cases have been reported to the Health Protection Agency, Colindale, London, to where specimens from patients suspected of having LGV are submitted for genotyping.7

This study was undertaken to ascertain clinic practices with respect to testing MSM for chlamydial infection and the management of men with proctitis.

METHODS

The study was carried out by the British Co-operative Clinical Group (BCCG), which was established in 1951 “for the immediate purpose of collecting information concerning venereal diseases from case records available in this country”. The broadening of the scope of clinical practice in clinics has been accompanied by a wider range of interest for the BCCG.

The study was a cross-sectional survey of all genitourinary medicine clinics in the United Kingdom, undertaken between July and September 2006. A questionnaire was sent to consultants in charge of each clinic through the BCCG’s network of regional representatives. When consultants were in charge of two or three clinics they only made a return for one clinic. The questions concerned clinical practice regarding testing MSM for chlamydial infection at different anatomical sites, the clinical procedures used in the investigation of MSM, the use of rectal smear microscopy, and the treatment for rectal chlamydial infection.

Data were entered into a spreadsheet and counts were made of relevant responses. Clinics were categorised according to whether they were associated with a teaching hospital or not, and by patient attendances estimated from the national GUM Waiting Times Audit.8

The protocol and questionnaire was reviewed and approved by the BCCG; ethical committee approval was not sought as the study did not include patient data.

RESULTS

A total of 185 questionnaires was distributed and 106 were returned, a response rate of 57%. Of the 106 questionnaires returned, 34 clinics (33%) were associated with a teaching hospital.

The majority of clinics reported that their laboratories used NAAT such as polymerase chain reaction (61, 58%), single-strand displacement assay (26, 25%) and transcription-mediated amplification (5) tests for chlamydia from urogenital and extragenital sites. Others used enzyme immunoassay (EIA, 12) or culture (3).

The numbers of clinics offering any testing for chlamydia, and the indications for urethral, pharyngeal and rectal testing are shown in table 1. Almost all clinics offered routine screening for urethral chlamydia, the majority (63, 59%) for rectal, and a minority (27, 26%) for pharyngeal. Testing was not available even for diagnostic or contact purposes for rectal chlamydia in 15 clinics (14%) and for pharyngeal infection in 68 (64%). Table 2 shows the geographical distribution of the responders.

Clinics that did not provide testing for rectal chlamydiae were smaller, with a median of 56 new patient attendances per week (range 27–79), compared with a median of 98 attenders (range 19–395) for those clinics offering such a service. In the majority of clinics, rectal chlamydial testing among MSM was introduced in the two years preceding the study (37 (59%) of the 62 clinics that provided the data).

Anoscopy was available for MSM in 99 clinics (93%), with most (59, 59%) offering anoscopy only to men with anorectal symptoms, the others undertaking this procedure at the initial attendance only (four clinics) or at each new episode of care (36 clinics).

Rectal smear microscopy was undertaken in 76 clinics (71%). In 29 clinics this was offered to all men, and in the remaining 47 it was undertaken only in symptomatic men. In 48 of the 76 clinics (64%) the number of cells in a defined microscopical field was counted, but in eight the number of cells considered diagnostic of proctitis was not stated. Figure 1 shows the number of cells per unit area that was considered diagnostic of proctitis by clinicians in these 40 clinics. (Tests for rectal gonorrhoea were undertaken in men with proctitis who attended each of these clinics, and for chlamydiae in 36 of these 40 clinics (90%).)

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Figure 1 Number of cells per unit area considered to be diagnostic of proctitis in the 40 clinics in which anal smear microscopy was performed.

Clinics had varied protocols for microbiological investigation in men with symptoms of proctitis. Fifty-nine clinics (56%) tested for the four common causes, namely Neisseria gonorrhoeae, Chlamydia trachomatis, Treponema pallidum and herpes simplex virus. A further 40 clinics tested for the first three pathogens, including 17 who also tested for herpes simplex virus if there was peri-anal or rectal ulceration. Seven clinics did not test for rectal chlamydia in men with proctitis.

Table 3 shows the treatment regimens used for chlamydia in men with and without symptoms of proctitis. In the 91 clinics that tested for and treated rectal chlamydial infection, 37 (40%) undertook a test of cure. Specimens were submitted for genotyping of chlamydial DNA to the Health Protection Agency laboratory from 75 clinics (71%). Thirty clinics (28%) had written protocols for the management of proctitis among MSM.

DISCUSSION

We have found a lack of consistency in the indications for chlamydia testing in MSM, and a wide range of laboratory methods in use. The majority of laboratories serving UK clinics use a NAAT for the diagnosis of genital chlamydial infection, as recommended by the UK National Screening and Testing Guidelines.9 10 Others employ tests that are not compatible with good clinical and diagnostic practice. Although tissue culture is the only test accepted as a first choice for the detection of rectal chlamydial infection,9 few clinics have access to this method, and most laboratories that test for infection at this anatomical site use a NAAT. Such tests have not, however, been licensed for use on rectal specimens although data supporting the validity of NAAT for rectal specimens are available.11^–13 Although EIA is not licensed for use on rectal material because of crossreactivity with other organisms,14 four clinics used this method for the detection of rectal infection. Several respondents noted that their local laboratory would not process rectal specimens either because of lack of validation of the NAAT used by that centre, or because the laboratory used an EIA for chlamydial detection. These clinics had relatively few attenders compared with the clinics that provided rectal chlamydial testing.

Despite concerns about the specificity of NAAT on rectal material, many clinics in the United Kingdom either screen routinely for infection in MSM or test selected men. This practice has only recently been introduced, principally as a result of the emergence of LGV proctitis based on the genovar L of LGV. Although the majority of men with rectal infection with the genotype trachomatis are symptomless,15 inflammatory changes that may increase the risk of HIV transmission can be identified.16 There is also the possibility of transmission of chlamydiae to the urethra of the sexual partner, therefore the identification and treatment of infected individuals may be justified. Infection with the LGV genotype often causes severe proctitis, although symptomless cases are not uncommon.17

The apparently low response rate from teaching hospitals reflects the fact that many UK clinics are not associated with a teaching hospital.

Microscopy of stained smears of rectal material was undertaken in approximately three-quarters of clinics, most frequently in MSM with anorectal symptoms. The identification of Gram-negative diplococci permits a presumptive diagnosis and therefore prompt treatment of rectal gonorrhoea,18 and Gram-smear microscopy is recommended for this purpose in men with clinical features of proctitis.19 The value of microscopy in making a diagnosis of proctitis, however, remains uncertain. In 64% of the clinics that undertook microscopy the number of polymorphonuclear leukocytes per unit area was recorded. There was, however, marked variation between clinics in the number of cells that was considered diagnostic of proctitis (fig 1). Little has changed since the survey of clinic practices undertaken by Adler20 in the late 1970s. In a study that compared cytological and histological findings, McMillan et al21 found that there was a good correlation between the finding of more than 10 polymorphonuclear leukocytes per unit area (0.64 cm2) and histological changes of acute proctitis. In that study, however, a defined area of mucosa was sampled, and so the results cannot be extrapolated to “blind” sampling used in many clinics. It must be questioned whether it is necessary to enumerate the cells if there is obvious mucopus in the rectal lumen. In any case, in the majority of these clinics, tests for gonorrhoea and chlamydiae were undertaken in men with suspected proctitis.

In most clinics, symptomless rectal chlamydial infection was treated by the same regimens used in uncomplicated genital tract infection.22 There are no data, however, to inform as to whether such regimens are appropriate for infection at this anatomical site. Similarly, definitive studies on the treatment of LGV proctitis have not yet been reported. Guidelines for the management of LGV recommend treatment with doxycycline 100 mg twice a day, tetracycline 500 mg four times per day, or erythromycin 500 mg four times per day, all for 21 days.19 20 This survey has shown that only 58% of clinics use these regimens in the treatment of symptomatic chlamydial proctitis. There is no published guidance on whether a test of cure for rectal infection is necessary. As treatment is still empirical, however, it seems reasonable to undertake one test of cure, particularly in the case of LGV proctitis. Over 40% of clinics that offer rectal testing already undertake such a test. Clearly, studies on the optimal management of rectal chlamydial infections are needed.

More than one-third of clinics offered testing for pharyngeal chlamydial infection. This was surprising because of the low prevalence of infection at that anatomical site, even among individuals at high risk of infection.25

This study shows the urgency of standardising the diagnosis and management of chlamydial infection in MSM. In collaboration with the British Association for Sexual Health and HIV, we aim to (a) produce updated guidance on the diagnosis of chlamydiae in MSM especially from rectal specimens; (b) encourage the submission of further data on the validation of rectal NAAT for chlamydia diagnosis to provide evidence for licensing in the United Kingdom; and (c) follow up clinics still offering EIA to encourage switching to NAAT.