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Epidemiology
Original research
Mycoplasma genitalium coinfection in men with symptomatic gonococcal urethritis
  1. Daniel Richardson1,
  2. David A Lewis1,2,
  3. Neisha J Jeoffreys3,
  4. Deborah L Couldwell1,2
  1. 1 Western Sydney Sexual Health Centre, Western Sydney Local Health District, Parramatta, New South Wales, Australia
  2. 2 Marie Bashir Institute for Infectious Diseases and Biosecurity and Westmead Clinical School, Faculty of Medicine and Health, The University of Sydney, Sydney Medical School, Westmead, New South Wales, Australia
  3. 3 Department of Microbiology, Institute of Clinical Pathology and Medical Research, Westmead, New South Wales, Australia
  1. Correspondence to Dr Daniel Richardson, Brighton & Sussex Medical School, Brighton, UK; daniel.richardson7{at}nhs.net

Abstract

Objectives International guidelines recommend Mycoplasma genitalium testing, preferably using an assay to detect macrolide resistance-associated mutations, for men presenting with non-gonococcal urethritis, but there is no specific guidance on such testing for men with gonococcal urethritis.

Methods This study aimed to estimate the proportion of men with gonococcal urethritis who have coinfection with M. genitalium through a retrospective analysis of cases of symptomatic urethral gonorrhoea at Western Sydney Sexual Health Centre in 2017 and 2018.

Results Fourteen of 184 (7.6%, 95% CI 3.7 to 11.5) men with gonococcal urethritis had M. genitalium detected in the urine at the time of presentation. No demographic or behavioural factors predicted M. genitalium coinfection. Coinfection with urethral Chlamydia trachomatis was detected in 29 of 184 (15.8%, 95% CI 10.5 to 21.1). All five men with macrolide-resistant M. genitalium detected returned for treatment with moxifloxacin at a median of 8 days (range 5–16 days) after presentation and treatment of gonorrhoea; three of five were documented to remain symptomatic at this visit.

Conclusion Although M. genitalium coinfection is less common than chlamydia among men with symptomatic gonococcal urethritis, M. genitalium testing, using an assay to detect macrolide resistance, will potentially reduce symptom duration particularly for men with macrolide-resistant infections, but may not be justifiable on cost-benefit analysis.

  • Mycoplasma
  • Neisseria gonorrhoeae
  • men
  • epidemiology (clinical)

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information. Due to the nature of this research, participants of this study did not agree for their data to be shared publicly, so supporting data are not available.

https://doi.org/10.1136/sextrans-2020-054529

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    Introduction

    Mycoplasma genitalium is an emerging bacterial STI and an increasingly common cause of non-gonococcal urethritis (NGU) and persistent/recurrent NGU in men.1 The prevalence of asymptomatic male urethral M. genitalium infection ranges from 1.2% to 3.9% in community-based populations, to 8.8% in those attending clinical services.2–5 It is thought that most men with urethral M. genitalium are asymptomatic, and that only a small proportion develop symptoms.1–6 Increasing M. genitalium macrolide resistance, particularly among men who have sex with men (MSM), is thought to be driven by use of azithromycin for treatment of STIs, while M. genitalium has not met the criteria needed to recommend screening of asymptomatic populations.2 4 7 Most guidelines currently recommend M. genitalium testing in men with symptomatic NGU; European guidelines recommend M. genitalium testing for men with urethritis, not further specified; however, there is no specific guidance on M. genitalium testing for men with gonococcal urethritis.7–10 The UK BASHH guidelines for gonorrhoea have recently changed to omit the use of azithromycin with ceftriaxone in order to reduce macrolide resistance to both Neisseria gonorrhoeae and M. genitalium.11 The UK BASHH guidelines for M. genitalium do not advocate the use of a single dose of azithromycin due to concerns about M. genitalium macrolide resistance.7

    N. gonorrhoeae infection is an important cause of urethritis and is estimated to affect 87 million people per year globally, with rising rates particularly in MSM.12 Following the introduction of antibiotics for the management of gonorrhoea in the 1930s, N. gonorrhoeae has acquired resistance to most classes of antibiotics used for treatment. Most countries currently use ceftriaxone plus azithromycin for empirical treatment of gonorrhoea.12 There is currently debate about the risks and benefits of using azithromycin as dual therapy for gonorrhoea due to increasing macrolide resistance and lack of new effective antimicrobials in the pipeline, as well as its potential effect on undiagnosed infections including M. genitalium.13–15

    Epidemiological research has so far focused on the prevalence of M. genitalium in asymptomatic men, and men with non-gonococcal and non-chlamydial urethritis. Small studies of men with urethritis have suggested that 2.4%–5.6% of men with gonococcal urethritis are coinfected with M. genitalium.16–18 However, we do not currently know the prevalence of M. genitalium in men with symptomatic urethral gonorrhoea in our population. Given the increasing rates of M. genitalium and both M. genitalium macrolide and quinolone resistance, it is important to consider how azithromycin treatment for men with gonococcal urethritis might affect M. genitalium coinfection, and whether such coinfection might lead to postgonococcal urethritis if left undetected and untreated. The primary aim of this study was to estimate the proportion of men presenting to our clinic with gonococcal urethritis who have coinfection with M. genitalium.

    Methods

    Study population and laboratory tests

    This is a cross-sectional analysis of cases of symptomatic gonococcal urethritis in men attending the Western Sydney Sexual Health Centre between January 2017 and December 2018. A sample size of 163 was calculated to estimate the prevalence, assuming a true prevalence of up to 12%, with precision of 0.05, at a confidence level of 0.95. Approximately 100 cases of symptomatic gonococcal urethritis per year are seen at the clinic, which provides comprehensive testing and management of STIs, including HIV, to priority populations in Western Sydney. Participant informed consent was not sought as the study was retrospective, and all testing and treatment, including for M. genitalium, were according to clinic guidelines. Men with asymptomatic urethral gonorrhoea were excluded as M. genitalium testing is not recommended for asymptomatic men. Gonococcal urethritis was defined as having urethral symptoms of discharge and/or dysuria with a positive nucleic acid amplification test and/or culture for N. gonorrhoeae within the study period. The men all had a sexual history taken, were examined by a sexual health nurse or physician, and had urethral swab collected and applied immediately onto modified Thayer-Martin medium for gonorrhoea culture. Men with urethral discharge also had Gram stain microscopy of urethral smear. First pass urine was collected for N. gonorrhoeae and Chlamydia trachomatis DNA detection (BD ProbeTec Strand Displacement Assay, Becton, Dickinson, Macquarie Park, Australia). All positive urine N. gonorrhoeae results were confirmed using the BD MAX GC rt PCR assay (Becton Dickinson), which uses a different nucleic acid target. As testing protocols changed during the study period, two different assays to detect M. genitalium DNA were used, either an inhouse PCR assay targeting mgpB, or from February 2018, ResistancePlus MG assay (SpeeDx, Eveleigh, Australia).19 Extragenital testing for N. gonorrhoeae and C. trachomatis from oropharyngeal and anorectal swabs was also done in MSM. Men were treated for urethral gonorrhoea with ceftriaxone 500 mg intramuscularly and azithromycin 1 g on the day of presentation if Gram-stained urethral smear detected Gram-negative intracellular diplococci. Men who tested positive for M. genitalium were either recalled for treatment with moxifloxacin if macrolide-resistant M. genitalium was detected, or awaited a test of cure (TOC) after 2–4 weeks if macrolide-sensitive M. genitalium was detected or no resistance information was available.

    Data were extracted from clinical records on age, sexual behaviour, including number and gender of sexual partners in the last 3 months, condom use for penetrative vaginal and anal intercourse in the last 3 months, HIV status, current use of HIV pre-exposure prophylaxis, and results of testing for N. gonorrhoeae, M. genitalium and C. trachomatis.

    Data were analysed using Stata V.12 statistical software. Bivariate associations were examined using χ2 or Fisher’s exact test, and OR, 95% CI and p values calculated using the Mantel-Haenszel method.

    Results

    Between January 2017 and December 2018, 208 men with symptomatic gonococcal urethritis were seen at the clinic, and 184 (88.5%) were also tested for M. genitalium in the urine. The 24 men who were not tested for M. genitalium due to clinician oversight were not significantly different from those tested for M. genitalium in terms of age, sex of partners, condom use and proportion testing positive for C. trachomatis. The median age was 31 years (IQR 24–38), and 109 of 184 (59.2%) were MSM, of whom 5 were known to be HIV seropositive. In the last 3 months, the median number of female partners for heterosexuals was 2 (range 0–20), and for MSM was 4 (range 0–50). Fourteen of 184 (7.6%, 95% CI 3.7 to 11.5) men with gonococcal urethritis had M. genitalium detected in the urine at the time of presentation, of whom 7 were MSM. M. genitalium coinfection was not significantly associated with any of the study factors (table 1). Coinfection with urethral C. trachomatis was detected in 29 of 184 (15.8%, 95% CI 10.5 to 21.1); there were no significant factors associated with urethral C. trachomatis and N. gonorrhoeae coinfection. One man had all three micro-organisms detected.

    View this table:
    Table 1

    Univariate associations with urethral Mycoplasma genitalium in men with urethral gonorrhoea

    Detection of extragenital N. gonorrhoeae in MSM with symptomatic urethral gonorrhoea occurred frequently: 38 of 101 (37.6%) had anorectal gonorrhoea and 32 of 101 (31.7%) had oropharyngeal gonorrhoea. Among MSM, anorectal C. trachomatis infections were detected in 10 of 101 (9.9%) and oropharyngeal C. trachomatis infections in 6 of 101 (5.9%). Of the 14 men with M. genitalium coinfection, 10 had available macrolide resistance test results and half of the infections (5, 50%) were macrolide-resistant (figure 1). Among heterosexual men with resistance results available, 4 of 5 (80%) had macrolide-susceptible strains, and among MSM 4 of 5 (80%) had macrolide-resistant M. genitalium. All five men with macrolide-resistant M. genitalium detected returned for treatment with moxifloxacin at a median of 8 days (range 5–16 days) after presentation and treatment of gonorrhoea; three of five were documented to be symptomatic at this visit, one was asymptomatic, and symptoms were not recorded for one man. Of the five men with macrolide-sensitive M. genitalium (who had all been given 1 g of azithromycin as part of their gonorrhoea treatment), two had negative TOC at 14 and 28 days, and three did not return for follow-up. Of four men with no macrolide resistance result, three had negative TOC between 34 and 100 days after treatment for gonorrhoea, and one was lost to follow up.

    Figure 1
    Figure 1

    Flow chart of Mycoplasma genitalium testing and results in men with gonococcal urethritis.

    Discussion

    We have estimated the prevalence of urethral M. genitalium in men in our population with symptomatic gonococcal urethritis to be 7.6%. We believe that this is the first study to estimate the prevalence of urethral M. genitalium in a large series of men with symptomatic gonococcal urethritis. Other studies in populations of symptomatic men have found that between 2.4% and 5.5% of men with urethral gonorrhoea have M. genitalium coinfection; however, the numbers of men with gonorrhoea were small and the studies were not powered to estimate M. genitalium prevalence.17–19

    We did not find specific risk factors associated with M. genitalium infection among the men with gonococcal urethritis. Although most men with urethral gonorrhoea have symptoms of urethritis, it is likely that only a small proportion of men with urethral M. genitalium infection have symptoms.1 6 20 All of the men in this study had symptoms of urethritis, most likely attributable to N. gonorrhoeae alone, but we were unable to evaluate whether M. genitalium infection contributed to symptoms and signs in some cases. Where macrolide resistance status was known, half of the men had macrolide-sensitive strains which resolved after treatment with azithromycin 1 g on the day of presentation with gonorrhoea. All these men later had negative TOC, as did three of the four men whose M. genitalium assay did not include macrolide resistance detection and who returned for TOC. However azithromycin 1 g has a significant failure rate and is no longer considered appropriate treatment for M. genitalium.8 It is believed that failure to test for M. genitalium prior to treatment with azithromycin 1 g and then undertake a TOC is an important driver of macrolide resistance.10 21 For men with macrolide-resistant M. genitalium, most of whom were symptomatic 5–16 days after receiving treatment for gonorrhoea, testing for presence of M. genitalium and use of the macrolide resistance assay potentially reduced the symptom duration. It should however be noted that the absolute number of men with N. gonorrhoeae and M. genitalium coinfection was only 14; further larger studies are needed to identify risk factors and the clinical relevance of M. genitalium testing and treatment in men with gonococcal urethritis.

    Where facilities for Gram stain of urethral smear to make a presumptive diagnosis of gonorrhoea in men presenting with urethritis are not available, clinicians use syndromic treatment, or wait for results of testing before treatment, and M. genitalium testing is recommended where resources allow. Specialist STI services with the facilities to presumptively diagnose and treat gonococcal urethritis at presentation need to assess the risk-benefit of M. genitalium testing in men with gonococcal urethritis, including local prevalence of coinfection and M. genitalium macrolide resistance, likelihood of symptomatic M. genitalium, potential adverse effects of treatment, contact testing and treatment of partners, and the cost of M. genitalium testing. At our centre, the cost of testing all 184 men with gonococcal urethritis for M. genitalium was approximately $A6600, compared with $A180 if testing for M. genitalium had been limited to men with persistent urethral discharge at follow-up. Although M. genitalium is a cause of urethritis in men, and cervicitis and pelvic inflammatory disease in women, most infections are asymptomatic and have not been associated with long-term sequelae. Asymptomatic screening aiming to reduce M. genitalium prevalence is not recommended.1 7

    The prevalence of urethral M. genitalium in our population with gonococcal urethritis was approximately half that of urethral C. trachomatis. However, while we expect that most urethral chlamydia will be cured by azithromycin 1 g, any macrolide-resistant M. genitalium infections will not, and a small proportion of macrolide-sensitive infections will develop macrolide resistance following treatment with azithromycin 1 g.22 If M. genitalium testing is not done at the time of presentation with gonorrhoea, waiting for men with M. genitalium postgonococcal urethritis to return for specific M. genitalium testing and treatment may lead to delay in diagnosis and effective treatment, and will increase the risk of loss to follow-up and reinfection by an untreated sexual partner and delayed detection of emergent macrolide resistance, with consequent further transmission of infection. The continued use of azithromycin in the empirical management of gonorrhoea is likely contributing to increasing antimicrobial resistance in M. genitalium, but the relative contribution of urethral M. genitalium infection to this effect is likely to be less than that of extragenital M. genitalium infection, as asymptomatic anorectal M. genitalium infection is common among MSM and asymptomatic testing is not recommended. Testing and treatment of C. trachomatis among men with gonococcal urethritis are established practice; however, whether such testing for M. genitalium is justified also needs to consider the potential sequelae of untreated infection for any partner/s. The risk of women developing complications is believed to be low, although female partners may be at small risk of cervicitis and pelvic inflammatory disease; the risk of harm for male partners of MSM is likely to be less, as M. genitalium has not been demonstrated to cause epididymo-orchitis and evidence in the case of proctitis is conflicting.23–26 BASHH guidelines recommend contact tracing and treatment for current partners in order to reduce the risk of reinfection.7

    Our study has several limitations. This is a single-centre study from an urban population in Sydney, Australia, and the results do not necessarily define the proportion of N. gonorrhoeae–M. genitalium coinfection in other settings. The M. genitalium assay changed during the course of the study; however, inhouse laboratory validation found 100% concordance for results of M. genitalium detection between the two methods. Although the study population was large enough to estimate prevalence in our population, it may have been underpowered to identify potential risk factors for coinfection. Furthermore, the absolute number of men with N. gonorrhoeae and M. genitalium coinfection was too small to determine the clinical relevance of M. genitalium coinfection and treatment. We were not able to assess whether men with N. gonorrhoeae and M. genitalium coinfection had symptomatic M. genitalium urethritis and if they warranted treatment for M. genitalium.

    In conclusion we have found that 7.6% of men presenting with symptomatic gonococcal urethritis also have urethral M. genitalium infection, but we were unable to identify any factors associated with coinfection. The use of single-dose azithromycin in men with gonorrhoea drives the development of antimicrobial resistance and is no longer recommended in some regional guidelines. If resources are available, M. genitalium testing, including detection of macrolide resistance mutations, in men presenting with symptomatic urethral gonorrhoea may benefit some men with macrolide-resistant M. genitalium coinfection by facilitating early diagnosis and treatment and reducing the symptomatic period. However, given the small chance that a detected M. genitalium infection is contributing to symptoms in this context, testing is not justifiable on cost-benefit criteria.

    Key messages

    • We do not know what the prevalence of Mycoplasma genitalium is in men with symptomatic gonococcal urethritis.

    • There is no clear consensus on testing for M. genitalium in men with gonococcal urethritis.

    • We have estimated that the prevalence of M. genitalium in men with gonococcal urethritis is 7.6% in our population

    • The contribution of M. genitalium to symtoms in men with gonococcal urethritis remains unclear.

    • Routine testing for M. genitalium in men with gonococcal urethritis may be important particularly in reducing transmission of macrolide resistance but requires significant resource.

    Data availability statement

    All data relevant to the study are included in the article or uploaded as supplementary information. Due to the nature of this research, participants of this study did not agree for their data to be shared publicly, so supporting data are not available.

    Ethics statements

    Ethics approval

    Ethics approval was obtained from the Western Sydney Local Health District Human Research and Ethics Committee (ref: 2019/ETH13052).

    Acknowledgments

    We would like to acknowledge the contribution to this research of the multidisciplinary sexual health team at Western Sydney Sexual Health Centre.

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    Footnotes

    • Handling editor Henry John Christiaan de Vries

    • Contributors DLC and DR designed the study. DLC collected and analysed the data. NJJ supervised the microbiology reporting. All authors contributed to the final manuscript.

    • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

    • Competing interests None declared.

    • Provenance and peer review Not commissioned; externally peer reviewed.