Abstract
Russia and Eastern Europe have the fastest growing HIV epidemic in the world. As sexually transmitted infections (STIs) play an important role in HIV transmission, we conducted this study to find the prevalence of three microorganisms associated with STIs in Arkhangelsk Oblast, Russia. First void urine from 1729 participants was analysed using nucleic acid amplification testing, and all participants completed a questionnaire. One hundred and twelve (6.5%) were tested positive for Chlamydia trachomatis, 67 (3.9%) for Mycoplasma genitalium and 221 (12.8%) for Ureaplasma urealyticum. A significant association was found between C. trachomatis and U. urealyticum (odds ratio [OR] 1.85; 95% confidence interval [CI] 1.1 to 3.0). U. urealyticum was associated with similar social demographics and sexual risks as C. trachomatis and M. genitalium. This suggests that U. urealyticum has a possible role as an STI pathogen or might be a contributing factor for the spread of other STIs.
INTRODUCTION
As a result of the breakup of the Former Soviet Union (FSU), Russia has gone through major changes, including changes to the health-care system. The prevalence of different communicable diseases including sexually transmitted infections (STIs) increased during the 1990s. 1–3 FSU had the fastest growing HIV epidemic in the world during the last decade, primarily driven by intravenous drug users (IDUs). 4 The major transmission route for HIV in Russia and Eastern Europe is among IDUs. 5 However transmission routes of HIV are changing towards more sexual transmission. 6–8 Control of STIs is essential to reduce further spread of HIV, as they may increase the risk of both acquisition and transmission. 9,10
Non-gonococcal urethritis (NGU) and cervicitis is primarily associated with Chlamydia trachomatis and Mycoplasma genitalium, and less frequently with Trichomonas vaginalis, herpes simplex virus, adenovirus or Haemophilus species. Still, the aetiology of 25–40% of NGU cases is unknown. 11,12 Ureaplasma urealyticum has been associated with acute and chronic NGU, but its role as a pathogen is still debated. 11,13–16
Proper laboratory diagnostic methods are essential for controlling STIs, and these have been lacking in Russia and Eastern Europe, 17,18 resulting in uncertain data regarding incidence and prevalence for most STIs in the region. Validation of Russian nucleic acid amplification tests (NAATs) for diagnosing STIs, shows that these are comparable to internationally acknowledged methods. 17–19 Internationally published prevalence data based on proper diagnostic methods for STIs in Russia and Eastern Europe are limited.
This study aimed to map the prevalence of C. trachomatis, M. genitalium and U. urealyticum in clinical and non-clinical settings in Arkhangelsk Oblast, Russia, using validated NAATs.
MATERIALS AND METHODS
Study population
The study population (n = 1729) was recruited as five different subpopulations in Arkhangelsk Oblast from November 2007 to May 2008. Outpatients at the HIV centre and the STI clinic were invited to participate during the recruitment period. The third group was university students through general information from health-care workers at the universities. The fourth group was recruited among military recruits by health-care workers at a military hospital. The last group was women seeking abortion, invited during the recruitment period from different hospitals in Arkhangelsk. The male/female ratio was 0.9, and more than 60% of the study population was under 30 years old. The participants completed a questionnaire about social demographic and sexual risk behaviour characteristics. Self-reported symptoms were discharge, dysuria, rash, itching, lesions or blisters, dyspareunia and lower abdominal pain. Participation was voluntary and all participants provided written informed consent.
Clinical and laboratory methods
First void urine of 5–10 mL from the participants was analysed for C. trachomatis, M. genitalium and U. urealyticum DNA with Russian commercial kits (Inter Laboratory Services, Moscow, Russia) using a Rotor-Gene 6000 Real-Time PCR Machine (Qiagen, Hilden, Germany). The Russian kits for the detection of C. trachomatis and M. genitalium have proven to be comparable to internationally validated commercial assays. 17,18 The analytical sensitivity (detection limit) and specificity of the U. urealyticum kit are reported to be 5 × 103 geq/mL and 100% respectively, by the manufacturer (Alexander Guschin, unpublished data). The analytical specificity was determined after testing human DNA and 33 different bacterial species commonly found in the genital area, including four different Ureaplasma parvum and 13 different Mycoplasma species.
Analyses were performed at the Regional Hospital of Dermatovenereology, Arkhangelsk.
Participants testing positive for C. trachomatis and M. genitalium were treated with azithromycin 1 g stat and U. urealyticum-confirmed patients were treated with clarithromycin 500 mg × 2 for 10 days. All diagnosis and treatment were given free of charge.
Statistical methods and analysis
Data were analysed using SPSS 16.0 for Mac (SPSS, Chicago, IL, USA). Odds ratios (ORs) with 95% confidence intervals (CIs), estimated by means of binary logistic regression were used to measure the associations of social, demographic and sexual risk characteristics between non-infected and infected participants. ANOVA analysis of variance and Bonferroni post hoc risk tests were used to calculate the significant differences between groups.
Ethics
The study was approved by the Regional Ethical Committee (REK NORD) for Northern Norway, and the Medical Health Administration in Arkhangelsk Oblast, Arkhangelsk, Russia.
RESULTS
Demographics, sexual risk behaviour and prevalence of the three microorganisms according to gender
Actual numbers with percentages in brackets, if not otherwise specified
*Information on gender was missing for 13 participants
HIV = human immunodeficiency virus; CI = confidence interval
Prevalence of microorganisms (shown as actual numbers with percentages in brackets), based on recruitment groups
*Information on recruitment groups was missing for four participants
Prevalence of microorganisms (actual numbers with percentages in brackets) according to age groups
Correlation of positive tests to demographics, sexual risk behaviour and symptoms
OR = odd ratios; CI = confidence interval
Among the C. trachomatis-positive individuals, 23 (20.5%) also tested positive for U. urealyticum and eight (7.1%) tested positive for M. genitalium. Eleven (16.4%) M. genitalium-positive individuals also tested positive for U. urealyticum. A significant association between C. trachomatis infection and U. urealyticum positive test was found (OR 1.85; 95% CI 1.1–3.0). One individual tested positive for all three microorganisms.
Age, smoking status and age at first intercourse were significantly associated with all three organisms; the number of sexual partners during the last six months was significantly associated with C. trachomatis infection. The reported symptoms were significantly associated with C. trachomatis infection (OR 2.87; 95% CI 1.65–4.97) for men. For women, the reported symptoms were significantly associated with testing positive for M. genitalium (OR 2.55; 95% CI 1.10–5.90).
DISCUSSION
To our knowledge this is the first large study using validated NAATs to detect sexually transmitted microorganisms in Russia. There are few prevalence studies for these three microorganisms from non-clinical populations, and there are no official Russian figures for M. genitalium or U. urealyticum.
The prevalences of C. trachomatis, M. genitalium and U. urealyticum in the study population were high. For C. trachomatis the prevalence ranged from 3.8% among the military recruits to 14.9% in the student sub population. Such high prevalence is in sharp contrast to the official regional and national Russian chlamydia incidence rates for 2007 of 119.6/100,000 and 91.1/100,000, respectively. 20 In contrast, the Norwegian incidence rate for 2007 was 490/100,000. 21 This emphasizes the importance of adequate STI control, including proper diagnostic methods, surveillance and partner tracing.
A study conducted in Moscow using NAATs showed high prevalence of M. genitalium (26%) and C. trachomatis (33%) among STI patients. 22 The Moscow study recruited high-risk male patients who attended STI clinics, and can explain the elevated prevalence reported, compared with our results. M. genitalium prevalence in our clinical and non-clinical populations was 3.9% (ranging from 3.4 to 5.8%). U. urealyticum as a pathogen is debated. Despite the previous studies identifying the organism as the causative agent of acute and chronic NGU, U. urealyticum is predominantly regarded as a commensal. However, U. urealyticum was the most prevalent microorganism in our study (12.8%) and it was significantly associated with a positive C. trachomatis test.
Russia and Eastern Europe have the fastest growing HIV epidemic in the world, and a focus on STI diagnostics, treatment and prevention is therefore a crucial part of HIV prevention. 6,7,23,24 Our results confirm high prevalences of STI microorganisms in both clinical and non-clinical settings.
C. trachomatis and M. genitalium are highly prevalent in the study population and presumably elsewhere in Russia. This study emphasizes the urgent need for adequate diagnosis, prevention and control of STIs in Russia in order to improve reproductive health, and limit the spread of HIV in this region. U. urealyticum is associated with similar social demographics and sexual risks as C. trachomatis and M. genitalium. The significant association between C. trachomatis and U. urealyticum warrants further study concerning the role of U. urealyticum as a pathogen or a contributing factor to the transmission of STIs.
Footnotes
ACKNOWLEDGEMENTS
The authors thank Dr Ingeborg Lyngstad Vik, Olafiaklinikken, for valuable discussions and Professor Andrey Maryandeshev in making this study feasible.
The study was financially supported by Northern Norway Regional Health Authority, the Barents Secretariat, the Norwegian Ministry of Health and Care Services and the University of Tromsø.
All authors declare no conflicts of interest. The study was financially supported by Northern Norway Regional Health Authority, the Norwegian Barents Secretariat, the Norwegian Ministry of Health and Care Services and the University of Tromsø.