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Abstract
Background Men are not routinely tested for Trichomonas vaginalis (TV) and Mycoplasma genitalium (MG) in the Netherlands and, therefore, very few studies have looked into their prevalence and/or role in urogenital complaints in the Dutch male population.
Objective To describe the age-specific prevalence and disease burden of TV and MG, and their co-occurrence with Chlamydia trachomatis (CT), in men attending the sexually transmitted infections (STI) clinic in Amsterdam, the Netherlands.
Methods Urine samples and clinical data were collected from 526 men who have sex with women (MSW) and 678 men who have sex with men (MSM) attending the STI clinic. To investigate age as a risk factor, we oversampled older men. Urine samples were tested for TV and MG using molecular tests.
Results The overall prevalence was 0.5% (6/1204) for TV and 3.1% (37/1204) for MG. Four out of the six TV cases were older than 40 years and all TV cases were MSW. No age trend was observed for MG, nor did MG prevalence differ between MSW and MSM. Co-infections between TV or MG and CT were rare. TV infection did not associate with urogenital symptoms, whereas 5.9% of men reporting urogenital symptoms were infected with MG.
Conclusions TV infection was rare in men, asymptomatic and was limited to the heterosexual network. MG infection was relatively common and equally prevalent among MSW and MSM of all ages. Most MG infections remained asymptomatic, however, our results suggest that up to 6% of urogenital complaints could be explained by MG infection.
- NON SPECIFIC URETHIUS
- INFECTIOUS DISEASES
- MALES
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Introduction
Trichomonas vaginalis (TV) and Mycoplasma genitalium (MG) are common urogenital tract infections that are associated with vaginitis in women and non-gonococcal urethritis (NGU) in men.1 ,2 Both infections are also associated with adverse pregnancy outcomes and increased risk of HIV acquisition.1 Despite both infections being curable, men are not routinely tested for TV or MG in the Netherlands; this means that epidemiological data on male prevalence, or clinical spectrum, of these infections is limited. Also, TV infections are more common in older age groups,3 and as older age groups are less at risk for sexually transmitted infections (STIs) such as Chlamydia trachomatis (CT), they tend to be less studied in STI epidemiology.
Compared with other STIs, epidemiological research on MG is still in its infancy. This is probably due to the difficulty of culturing the organism and only recent advances in DNA amplification tests for MG have aided its detection. Now the bacterium is believed to explain approximately 20–35% of non-chlamydial NGU cases,4 making its detection meaningful.
Our objective was to describe the age-specific prevalence of TV and MG infections in an urban Dutch male population consisting of men who have sex with women (MSW) and men who have sex with men (MSM). Second, the possible association of TV and/or MG infections with male urogenital complaints (not caused by gonorrhoea), ethnicity and/or co-infections with CT or HIV was determined.
Methods
Our study was conducted at the STI clinic in Amsterdam, the Netherlands. All data used in this study was collected as part of routine management and anonymised before the analysis. We included 1204 men who attended the STI clinic from March to October 2014. As part of the STI clinic routine examination, 2 ml of first-catch urine was used for CT and Neisseria gonorrhea (NG) detection, and specifically for the study, these same samples were tested for TV using transcription-mediated amplification (APTIMA combo, Hologic). All samples were stored at −20°C and processed batchwise within a month of procurement. APTIMA tests were performed according to the manufacturer's protocol. TV APTIMA positive samples were confirmed by an inhouse real-time PCR. A validation experiment proved that this real-time PCR can indeed detect TV in male urine with a sensitivity of 102 parasites/mL (data not shown). For MG detection, DNA was isolated from 200 µL of the APTIMA urine sample by isopropanol precipitation. The real-time PCR targeting the MGPa gene was performed using primers published by Jensen et al.5 By design, we excluded clients that tested positive for NG in either Gram stain and/or APTIMA combo (n=41), as we aimed to study the clinical relevance of testing for TV and MG infections in men with NGU complaints.
To ensure an equal age representation in our study population, we included approximately 300 men in each of the following age categories: <30 years old; 30–39 years old; 40–49 years old, and; >50 years old. Difference in prevalence between groups was tested with the χ2 test. Reported clinical symptoms, age, ethnicity and HIV status, if known, were extracted from the electronic client file and subsequently anonymised, . Clients of the STI clinic are notified that remainders of samples may be used for scientific research, after anonymisation of client clinical data and samples. If clients object, data and samples are discarded.
Results
We included 1204 men in our study: 678 MSM and 526 MSW. The majority of the study population was Dutch. MSM were slightly older than MSW (median age of 41 (IQR: 31–51) years vs 37(IQR: 29–48) years, respectively; p<0.001), despite our efforts to include equal numbers of MSM and MSW per age category. MSM and MSW also differed with respect to STI risk: MSM reported more sexual partners in the previous 6 months compared with MSW (median of 6 (IQR: 3–15) vs 3 (IQR: 2–5), respectively; p<0.001).
Six out of 1204 (0.51%) urine samples, all from MSW, were found positive for TV. TV prevalence was highest in older (>50 years) MSW (2.6%). However, the sample size was too low to find a statistically significant correlation with age. The overall prevalence for MG was 3.1% (37/1204); 2.5% for MSW and 3.8% for MSM (p=0.13). No significant age trend for MG infection was observed.
Our study population had a CT prevalence of 5.9% (72/1204). Significantly higher CT prevalence was seen in MSW compared with MSM: 7.8% of MSW were CT positive, compared with 4.6% of the MSM (p=0.027). CT infection was most prevalent in the younger MSW age categories (p<0.001; table 1).
Prevalence of Trichomonas vaginalis, Mycoplasma genitalium and Chlamydia trachomatis infection in MSM and MSW in relation to age and ethnicity
A total of 266 men (22%) reported STI related symptoms, of which 135 men (11.2%) specifically reported urogenital symptoms (burning sensation and/or urethral discharge). Of those men specifically reporting urogenital symptoms, 1 (0.7%) had a TV/MG co-infection and 7 (5.2%) were infected with MG. In contrast, 24 men (17.8%) with urogenital symptoms had a CT infection. We found very few co-infections: apart from the one symptomatic TV/MG co-infection, only one asymptomatic CT/TV and one asymptomatic CT/MG co-infection were observed. Two MG and two CT cases were HIV-positive and these were all asymptomatic. Furthermore, all six men with TV infection were of non-Dutch ethnicity—half (n=three) were Surinamese, whereas MG infections occurred among different ethnicities, including: Dutch, Eastern European, Northern and Sub-Sahara African and Surinamese (table 1).
Discussion
This study showed that TV infection is rare in the Dutch male STI clinic population (0.5%), that it occurs mostly asymptomatic and that it limits itself to the heterosexual network. MG infection, on the other hand, is quite common (3.1%) in the heterosexual and homosexual networks and it is equally prevalent among all age groups. Up to 5.9% of men reporting urogenital symptoms—and who tested negative for NG and CT—were found to have an MG infection.
A previous study in the Netherlands describes a prevalence of 0.6% for TV in an STI cohort and 1.5% in a general practitioners cohort; all cases were women, but a lack of male cases could be explained by low male participation in their study.6 By comparison, the Amsterdam prevalence of TV infection in women attending the Amsterdam STI clinic in 2013 was 2.6% (STI clinic 2013 Annual Report). Nonetheless, the male prevalence of TV infection in Amsterdam remains very low, and much lower than prevalence reported elsewhere in men.3 The exact infection duration of TV in men is still unknown but is assumed to last at most a few weeks, compared with months in women.7 If indeed the infection duration is short in men, the parasite will be difficult to detect, especially in populations with very low prevalence rates such as the Netherlands.
No TV positivity was found among MSM, which is in line with a previous study evaluating racial disparities in HIV acquisition in the USA, that also found no TV infections in their MSM study population of over 500 MSM.8
MG infection has a prevalence rate second only to CT infection in this STI clinic study population and is equally prevalent in MSM and MSW. No specific age group seems to be at higher risk for MG infection and the infection was found across different ethnic groups. The overall prevalence reported here is similar to the findings of Dutch colleagues elsewhere in the country (van Alphen et al, unpublished data).
TV and/or MG infections were not associated with CT or HIV infections in our study population. Considering the rarity of TV, this is not surprising and this also supports the findings of Geelen et al6 who found no association between TV and CT infections. MG infection, however, is commonly prevalent in the absence of CT and seems to explain some non-chlamydial NGU cases. Other studies in the UK and USA, studying mostly symptomatic patients, report higher MG/CT co-infections rates and stronger associations between urethritis and MG than found here.2 ,9 This means that non-chlamydial NGU could be attributed to an infection with MG and should be treated accordingly. It is also important to keep in mind that treatment regimes for (recurrent) urethritis have especially been developed to combat NG and CT infections and may be less effective against MG.10
Our study is limited by its single study centre design and prevalence documented here could differ from other locations. Also, the low number of TV cases and very few symptomatic MG cases limited us in detecting strong associations. However, as most STIs are very often asymptomatic it was necessary to investigate TV and MG among symptomatic and asymptomatic men at risk for STIs in Amsterdam.
To conclude, TV infection was rare in men (0.5%) and, therefore, seems an unlikely candidate to explain urogenital complaints in sexually active men in the Netherlands. MG infection, on the other hand, was common (3.1%), not age-specific and correlated with 5.9% of non-chlamydial-NGU cases.
Acknowledgments
The authors thank Fred Zethof for testing all samples for TV and Sandra van den Broek for data management and anonymisation of the clinical data.
References
Supplementary materials
Abstract in Dutch
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
- Abstract in Dutch - Online abstract
Footnotes
Handling editor Jackie A Cassell
Contributors CvdV wrote the manuscript. MH was responsible for MG testing. SMB, MSvR and CvdV were responsible for design of the study. MSvR set up the database and MSvR and CvdV performed the statistical analyses. SMB and HJCdV supervised the overall study. All authors reviewed and approved the final article.
Funding This work was supported by the Public Health Service of Amsterdam (GGD Amsterdam), the Netherlands.
Competing interests None declared.
Ethics approval Ethics Committee of the Amsterdam Medical Centre of the University of Amsterdam (reference number W15_159 # 15.0193).
Provenance and peer review Not commissioned; externally peer reviewed.