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Concurrent Gonococcal and Chlamydial Infections Among Men Attending a Sexually Transmitted Diseases Clinic

Posted on: Wednesday, 1 June 2005, 15:00 CDT

Summary: The aim of this retrospective study was to determine the prevalence of Chlamydia trachomatis co-infection in men with gonorrhoea attending a sexually transmitted diseases clinic in Edinburgh, Scotland. During the study period, there were 660 cases of culture-proven gonorrhoea. Chlamydial DNA was detected in the urethra in 79 (31%; 95% confidence interval [CI], 25-37%) heterosexual men who have sex with women (MSW); the median age was significantly lower than those with gonorrhoea alone (24.0 versus 30.0; P < 0.0005). The prevalence of urethral chlamydial infection among MSW was significantly higher than among men who have sex with men (MSM) (32 [12%; 95% CI, 8-16%] of 268 MSM) (χ^sup 2^ = 27.21; P < 0.001). Sixteen (24%; 95% CI, 14-34%) of 68 MSM with rectal gonorrhoea had concurrent rectal chlamydial infection. The high prevalence of concurrent gonorrhoea and chlamydiae therefore warrants empirical treatment and/or testing for chlamydia in all men with urethral gonorrhoea.

Keywords: gonorrhoea, chlamydial infection, MSM

Introduction

As heterosexual men and women with gonorrhoea frequently have concurrent infection with Chlamydia trachomatis, the UK National Guidelines and the US Centers for Disease Control recommend treatment of individuals with gonorrhoea for presumed dual infection.1'2 There are, however, no specific recommendations for the presumptive treatment for chlamydiae in men who acquire gonorrhoea through homosexual contact. Some clinicians do not treat men who have sex with men (MSM) for possible chlamydial infection because studies in the 1970s showed that the rate of detection by culture of C. trachomatis in the urethra of MSM who had gonococcal urethritis was significantly lower than that in heterosexual men (men who have sex with women [MSW]).3 However, more recent data from the USA, based on the detection of C. trachomatis by a ligase chain reaction (LCR) on urine samples, indicate that the prevalence of chlamydial infection in homosexual or bisexual men with urethral gonorrhoea (and, indeed, nongonococcal urethritis [NGU]) is similar to that of heterosexual men.4 Rectal infection with C. trachomatis is detected by nucleic acid amplification methods in up to 10% of men attending sexually transmitted diseases (STD) clinics,5 but little has been published on concurrent rectal gonococcal and chlamydial infections.

As the epidemiology of dual gonococcal and chlamydial infection, particularly among men, has not been studied extensively, it was the aim of this investigation to examine some characteristics of men with urethral and/or rectal gonorrhoea who attended a sexually transmitted infections clinic.

Methods

Patients

This was a retrospective study whose population consisted of all male patients who attended the Department of Genitourinary Medicine at the Edinburgh Royal Infirmary between 1 January 2000 and 27 November 2003 and who had culture-proven gonorrhoea. These men were identified from the database held within the STD/ Chlamydia Laboratory, Edinburgh Royal Infirmary, and their case-notes were retrieved by one of us (AMcM). Note was made of the age of the patient, ethnicity, gender(s) of his sexual partners, anatomical sites sampled for gonococcal and chlamydial infection and the results of these tests. The gender of the patients' partners was confirmed by examination of the records made by the health adviser to whom the individual had been referred for partner notification.

Clinical microbiological methods

Urethral material for Gram-smear microscopy and culture for Neisseria gonorrhoeae was taken using a 10 L plastic inoculating loop. The material for culture was inoculated directly onto plates of modified New York City medium (MNYC), which were then transported to the laboratory for routine processing. For the detection of rectal gonorrhoea, a cotton wool-tipped applicator stick was inserted through the anal canal into the distal rectum to a distance of about 3cm, rotated once, withdrawn and then used to inoculate a plate of MNYC. Pharyngeal specimens were obtained by swabbing the tonsils or tonsillar fossae using a cotton wooltipped applicator stick that was then used to inoculate a plate of MNYC.

In most cases, a first-voided urine specimen was taken for the detection of urethral chlamydial infection. When a man was unable to provide a urine sample, material was collected by passing a cotton wool-tipped wire swab, provided by the manufacturers of the test kit, about 4cm into the urethra, rotating once, and, after withdrawal, breaking the swab into the appropriate transport medium. For the detection of rectal chlamydiae, a cotton wool-tipped swab, provided by the manufacturers of the test kit, was inserted through the anal canal into the distal rectum to a distance of about 3cm, rotated once, withdrawn, and cut off into transport medium. Chlamydia-specific DNA sequences in the samples were sought by an LCR (LCx Abbott Diagnostics North Chicago, Illinois, USA) in the first 37 months of the study. All reactive specimens were rechecked and were only reported as positive if they were reactive on the repeat test. The material from rectal swabs that gave a positive LCR for C. trachomatis was tested retrospectively by the Roche COBAS Amplicor PCR test. The cross-examination of these methods was stopped after failure to record a single discordant result. From February 2003, urine, urethral and rectal specimens were tested for chlamydiae using the Roche COBAS Amplicor PCR test.

Statistical methods

The Mann-Whitney U and the χ^sup 2^ tests were used in the analysis of the numeric and categorical data, respectively, using the Statgraphics Statistical package.

Results

During the study period, there were 660 cases of culture-proven gonorrhoea: 267 cases among 254 MSW (11 men had two episodes and one man had three episodes), and 393 cases among 336 MSM (42 men, six men and one man each had two and three and four episodes, respectively); only one MSM gave a recent history of sex with women in the three months preceding his clinic attendance. There were four black African MSW and one Asian MSW; the other men were white.

Men who have sex with women

Of the 267 episodes in MSW, pharyngeal and urethral specimens for culture for N. gonorrhoeae were obtained from 165 men, and urethral material alone from 102 men. Of the former patients, pharyngeal infection was diagnosed in 15 (9.1%) men, in all but one case, in association with urethral gonorrhoea.

Among MSW, urethral or urine samples for the identification of C. trachomatis were not obtained from nine men, and the PCR was inhibited in a further four men; these 13 patients have been excluded from the analysis of concurrent urethral and gonococcal infection. From the remaining patients, urine or urethral swabs were obtained for PCR in 236 and 18 men, respectively; chlamydial DNA was detected in 79 (31%; 95% confidence interval [CI], 25-37%) men. The median age of the men with and without chlamydial infection was 24.0 years (interquartile range [IQR] 11.0 years) and 30.0 years (IQR 16.0 years), respectively, a difference that is significant (P < 0.0005). Figure 1 shows the prevalence of urethral chlamydial infection with respect to each age group.

Figure 1 Prevalence of chlamydial infection among men who have sex with women, and who have urethral gonorrhoea

Figure 2 Anatomical sites infected with N. gonorrhoeae among men who have sex with men

U = urethra; R = rectum; P = pharynx

Men who have sex with men

Material for culture for N. gonorrhoeae was obtained from the pharynx, urethra and anorectum in 376 (95.7%) MSM. The following specimens were obtained from the remaining patients: urethra and pharynx (10), urethra only (two), urethra and anorectum (two), and anorectum and pharynx (three). Figure 2 shows the infected anatomical sites in the 393 cases, the most common being the urethra (291 [74.0%] of 393 infections).

Amongst MSM, urine or urethral swabs for the detection of C. trachomatis were not taken from 17 men, and in two cases the PCR was inhibited; these 19 patients are excluded from further analysis of concurrent gonococcal and chlamydial urethral infection. Urethral swabs or urine samples were obtained from 13 and 363 MSM, respectively. C. trachomatis DNA sequences were detected in the urethra of 32 (12%; 95% CI, 8-16%) of the 268 men with urethral gonorrhoea, and from whom satisfactory chlamydial tests had been obtained. The median ages of men with and without urethral chlamydiae were 32.0 years (IQR 17.5 years) and 29.0 years (IQR 12.5 years), respectively, a difference that was not significant (P>0.05). Figure 3 shows the prevalence of urethral chlamydial infection with respect to age group.

Rectal material for chlamydia detection was obtained from 229 MSM, 72 of whom had rectal gonorrhoea. The PCR was inhibited in six cases, including four of the 72 men with rectal gonorrhoea. Chlamydiae were identified in the rectum of 16 (24%; 95% CI, 14- 34%) of the remaining 68 patients with rectal gonorrhoea. The median ages of men with and without concurrent rectal chlamydial and gonococcal infections were 23.0 (IQR 10.5 years) and 29.0 (IQR 12.0 years), respectively; this was not a significant difference (P>0.05).

Rectal chlamydial infection was also identified in 10 patients who had gonorrho\ea at an anatomical site other than the rectum: eight men had urethral gonorrhoea (two had concurrent urethral chlamydiae), two had pharyngeal gonorrhoea.

Comparison of results obtained from MSW and MSM

The prevalence of urethral chlamydial infection among MSW (31%) was significantly higher than among MSM (12%) (χ^sup 2^ = 27.21; P<0.001). The median age of MSW with concurrent urethral and gonococcal infection (24.0 years) was significantly lower than that of MSM with dual infection (32.0 years) (P < 0.05); there was, however, no significant difference with respect to the median age between urethral chlamydia-negative MSW (30.0 years) and MSM (29.0 years) (P>0.05).

Discussion

Our data confirm the findings of others that coinfection with C. trachomatis in young MSW with urethral gonorrhoea is common,6'7 and justify the recommendations to give empirical treatment for chlamydiae when treating urethral gonorrhoea in MSW. Most dual infections occurred in young men, the median age being 24,0 years. Creighton et al.,6 working in an STD clinic in London, also reported that the median age of men with dual infection (22.4 years) was lower than that of men with either gonorrhoea alone (27.9 years) or chlamydiae alone (26.5 years) (MSM and MSW were considered together in their analysis). As we did not examine the prevalence of chlamydiae in men without evidence of gonococcal urethritis, we cannot comment further on age differences between men with single or dual infection with chlamydiae. In our study, the prevalence of chlamydiae was highest in men aged between 20 and 24 years (Figure 2), and decreased thereafter. These findings are in accord with those of Stamm,8 who reported that the prevalence of chlamydiae in men with urethral chlamydial infection decreased in each 5-year period from age 19 to 39 years.

Figure 3 Prevalence of urethral chlamydial infection among men who have sex with men and who have urethral gonorrhoea

Until recently, it was generally acknowledged that the prevalence of urethral chlamydial infection among MSM was significantly lower than among MSW. This assumption was challenged, however, by Ciemins et al,,4 who reported that the prevalence of chlamydiae in MSM and MSW with NGU who attended an STD clinic in San Francisco was equivalent -18% and 20%, respectively. They also reported that chlamydia co-infection was significantly greater among MSM or bisexual men (15.2%) than among MSW (8.4%) with urethral gonorrhoea. Our data do not confirm this finding: significantly fewer MSM with urethral gonorrhoea were infected with C. trachomatis. Creighton et al.6 also reported that co-infection with chlamydia was less common in MSM than in MSW - 6.9% of 68 MSM compared with 24.2% of 512 MSW. The reasons for the discrepancy between the findings in the UK and those in the USA are not immediately apparent, but differences in the populations served by the clinics may be important. For example, more MSM in San Francisco than those in the UK may also have had sex with women - proportions of men who have sex with both men and women were not reported in Ciemins' paper. In our study, only one man gave a history of sex with women in the three months preceding his clinic attendance.

In this study of MSM with urethral gonorrhoea, there was no significant difference between the median ages of those with or without concurrent chlamydial infection, and the proportion of those with dual infection did not vary significantly between the age groups (Figure 3). This finding differs from those of others. Stamm8 noted a decrease in the rates of chlamydial infection from age 19 years, and Ciemins et al4 reported that young age (less than 24 years) was associated with chlamydial infection in MSM or bisexual men with urethritis. A reason proffered to explain the higher prevalence of chlamydiae among younger than older MSM is that past chlamydial infection confers resistance to re-infection. Studies undertaken in the 1970s that showed that the prevalence of serum antichlamydial antibody was high among MSM, but the isolation rate of C. tmchomatis was low, appear to support this hypothesis.8 If this is the case, it would infer that MSM in our geographical area do not acquire chlamydial infection in their youth, and therefore are not immune to infection as they age. The difference between our findings and those in the USA studies may be explained by differences in the sexual behaviour between the population groups. For example, fewer men in Southeast Scotland may have had sexual intercourse with women in their youth. In the absence of comparative data on sexual behaviour, however, this assumption is at most speculative.

The low proportion of screening for rectal chlamydial infection in this study is explained by the lack of a policy regarding such screening until early 2003. Upto that time, only three physicians routinely undertook testing for chlamydial infection at this anatomical site. However, it is not thought that the results are biased: these were consecutive patients attending the department, and had not been specially selected for study by any of the clinicians. The high prevalence of concurrent chlamydial infection in men with rectal gonorrhoea is a strong argument for testing for chlamydiae and/or giving empirical treatment to men in whom a diagnosis of rectal gonorrhoea is made or suspected. Most first- line treatments for anogenital gonorrhoea do not cure chlamydial infection, and so specific therapy needs to be given.9 The majority of rectal infections with the oculogenital serovars of C. trachomatis are symptomless, and local complications appear to be rare. Nevertheless, there is a case for treating infection at this anatomical site. Although data supporting a role for rectal chlamydial infection in facilitating transmission of HIV are lacking, chlamydial infection in women is recognized to do so.10 It therefore seems likely that rectal infection will also increase this risk.

As pharyngeal tests for C. trachomatis were not taken in our patients, the true prevalence of chlamydial infection in men with gonorrhoea has possibly been underestimated. However, other studies, using nucleic acid amplification methods for the detection of chlamydiae, have shown that pharyngeal infection among men, including MSM7 is low - less than 1%.11/I2 When resources are limited, it is therefore difficult to justify the inclusion of pharyngeal sampling for C. trachomatis in a screening programme.

References

1 Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines. MMWK 2002;51:36-12

2 Clinical Effectiveness Group (Association for Genitourinary Medicine and the Medical Society for the Study of Venereal Diseases. 2001 National Guideline on the Management of Gonorrhoea in Adults [www.mssvd.org.uk]

3 Bowie WR, Alexander ER, Holmes KK. Etiologies of postgonococcal urethritis in homosexual and heterosexual men; roles for Chlamydia trachomatis and Ureaplasma urealyticum. Sex Transm Dis 1978;5:151-4

4 Ciemins EL, Flood J, Kent CK, et al. Reexamining the prevalence of Chlamydia trachomatis infection among gay men with urethritis. Implications for STD policy and HIV prevention activities. Sex Transm Dis 2000;27:249-51

5 Manavi K, McMillan A, Young H. The prevalence of rectal chlamydia infection among men having sex with men attending GUM clinic in Edinburgh. M / STD AIDS 2004;15:162-4

6 Creighton S, Tenant-Flowers M, Taylor CB, Miller R, Low N. Co- infection with gonorrhoea and chlamydia: how much is there and what does it mean? lnt J STD AIDS 2003;14:109-13

7 Lyss SB, Kamb ML, Peterman TA, et al Chlamydia trachomatis among patients infected with and treated for Neisseria gonorrhoeae in sexually transmitted diseases clinics in the United States. Ann Intern Med 2003;139:178-85

8 Stamm WE. Chlamydia trachomatis infections of the adult In: Holmes KK, Sparling PF, Mardh P-A et al., eds. Sexually Transmitted Diseases. 3rd edn. New York: McGraw-Hill, 1999;407-22

9 Robinson AJ, Ridgway GL. Concurrent gonococcal and chlamydial infection: how best to treat. Drugs 2000;59: 801-13

10 Wasserheit JN. Epidemiological synergy. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis 1992;19:61-77

11 Winter AJ, Gilleran G, Eastick K, Ross JD. Comparison of a ligase chain reaction-based assay and cell culture for detection of pharyngeal carriage of Chlamydia trachomatis. J Clin Microbiol 2000;38:3502-1

12 Debattista J, Clementson C, Mason D, et al. Screening for Neisseria gonorrhoeas and Chiamydia trachomatis at entertainment venues among men who have sex with men. Sex Transm Dis 2002;29:216- 21

(Accepted 22 March 2004)

A McMillan1 MD FRCP, K Manavi1 MD MRCP and H Young2 DSc FRCPath

1 Department of Genitourinary Medicine, Edinburgh Royal Infirmary, Lothian University Hospitals NHS Trust, Lauriston Building, 39 Lauriston Place, Edinburgh EH3 9HA; 2 Scottish Neisseria gonorrhoeae Reference Laboratory, Directorate of Laboratory Medicine (Microbiology), Edinburgh Royal Infirmary, Edinburgh, UK

Correspondence to: Dr A McMillan

Email: a.amcmm@btopenworld.com

Copyright Royal Society of Medicine Press Ltd. May 2005

Source: International Journal of STD & AIDS

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