High Rates of Trichomonas vaginalis among Men Attending a Sexually Transmitted Diseases Clinic: Implications for Screening and Urethritis Management
- Department of Medicine, University of Alabama at Birmingham and Jefferson County Department of Health, Birmingham
- Reprints or correspondence: Dr. Jane R. Schwebke, 703 19th St., South Zeigler Research Building 239, Birmingham, AL 35294-0007 (Schwebke{at}uab.edu).
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Presented in part: 41st Interscience Conference on Antimicrobial Agents and Chemotherapy, Chicago, 16–19 December 2001 (abstract D-2254).
Abstract
Trichomonas is a cause of nongonococcal urethritis (NGU); however, studies of its prevalence in men have been hampered by the lack of sensitive diagnostics. DNA amplification allows for reappraisal of the extent of infection in men. Men attending a sexually transmitted diseases clinic were tested for trichomonas, chlamydia, and gonorrhea. The prevalence of these pathogens was 17%, 19.6%, and 17.7% respectively. In men with NGU, 19.9% were infected with trichomonas. These data have implications for treatment of NGU and control of trichomoniasis.
Trichomonas vaginalis, the most common curable sexually transmitted disease (STD) among American women, causes an estimated 5 million new cases annually and has had its clinical spectrum well described in numerous carefully conducted studies [1–3]. In women, infection with T. vaginalis has been suggested to be associated with adverse outcomes of pregnancy [4], pelvic inflammatory disease [5, 6], and increased risk for acquisition of human immunodeficiency virus (HIV) infection [7]. Wet mount microscopy of vaginal secretions is most widely used for trichomonas diagnosis in women, although culture is significantly more sensitive [8–10]. Polymerase chain reaction (PCR)-based assays also are becoming available [11–13]. In contrast, trichomonas infections are not routinely diagnosed in men because of the apparent limited ability of culture to detect the organisms in the male genital tract. There has been little recent evaluation of the prevalence or clinical spectrum of trichomoniasis in this group. More than a decade ago, Krieger et al. [2] used culture techniques to demonstrate a 6% prevalence of T. vaginalis infections among men seeking care at a Seattle STD clinic, as well as strong associations between infection and either a history of contact to a sex partner with trichomoniasis or nonchlamydial nongonococcal urethritis (NGU). Such rates are much lower than those among women attending STD clinics. As with most STDs, infection in women presupposes an infected male partner. On the basis of data showing significantly increased sensitivity of a PCR-based diagnostic test for T. vaginalis in men, compared with that of culture [14, we used this PCR assay to reevaluate the prevalence and clinical spectrum of trichomoniasis among men attending an urban STD clinic, especially its association with nongonococcal urethritis (NGU).
Materials and methods. Heterosexual men attending the Jefferson County Health Department (JCDH) STD Clinic, Birmingham, Alabama, for a 6-month period beginning in June 2001 for STD screening or symptom evaluation were invited to participate in this study. Study recruitment was limited to those men seen initially by 1 of 2 research nurses stationed at the clinic. The Institutional Review Boards of the JCDH and the University of Alabama at Birmingham approved the study. Men were excluded from participation if they had urinated in the previous hour or had taken antibiotics during the previous 14 days. Two urethral swabs were collected from each participant for Gram stain and trichomonas testing. After collection of swab specimens, an ∼20-mL first fraction-voided urine specimen was collected in premarked 50-mL sterile conical tubes and was processed on-site, alloquotting half for trichomonas testing and the other half for detection of Neisseria gonorrhoeae and Chlamydia trachomatis by ligase chain reaction (LCR). Specimens for gonorrhea and chlamydia LCR testing were stored at 4°C and were processed within 24 h.
LCR was done by use of Abbott Laboratories's LCx Probe System Kits for N. gonorrhoeae (no. 8A48-87) and C. trachomatis (no. 9B11-91), according to the manufacturer's directions for processing urine specimens. Positive LCR tests were repeated by use of both the initial reaction mixture and the original urine specimen, to confirm preliminary results. For T. vaginalis testing, 10 mL of urine was processed by centrifugation at 201 g for 5 min. The urine pellet was sent to the laboratory for PCR testing. PCR testing for T. vaginalis was performed on urethral swab and urine specimens by use of TV3/7 primers, as described elsewhere [12, 14].
Results. Specimens were collected from a case series of 300 men who fulfilled the study eligibility criteria. Among these 300 men, the prevalence of chlamydial and gonorrhea infections were 19.6% (59) and 17.7% (53) respectively, and the prevalence of T. vaginalis was 17% (52) (table 1). Overall, 127 (42%) of the study participants were infected with at least 1 of the STDs. Of these 127 participants, coinfection with gonorrhea and chlamydia was present only in 17 (13.4%), coinfection with gonorrhea and trichomonas only in 12 (9.4%), coinfection with chlamydia and trichomonas only in 14 (11%), and infection with all 3 pathogens was present in 6 (4.7%).
Figure 1.
Distribution of mucosal sexually transmitted diseases (STDs) among men with (+) and without (−) evidence of urethritis
Table 1.
Prevalence of sexually transmitted disease (STD) pathogens among men attending an STD clinic.
Table 1 shows the prevalence of C. trachomatis, N. gonorrhoeae, and T. vaginalis in the study population, stratified by the presence or absence of symptoms. Men complaining of urethral discharge or dysuria were significantly more likely to have an STD than those who were asymptomatic (88 [56.1%] of 155 vs. 39 [26.9%] of 145; P<.001; relative risk [RR], 1.8; 95% confidence interval [CI], 1.4–2.2). For chlamydial or gonorrheal infection, there also were statistically significant differences in prevalence rates between symptomatic and asymptomatic individuals (41 [26.4%] of 155 vs. 18 [12.4%] of 145; P=.002; RR, 1.5; 95% CI, 1.2–1.8 for chlamydia; and 48 [31%] of 155 vs. 5 (3.4%) of 145; P<.001; RR, 2.1 [95% CI, 1.8–2.5] for gonorrhea). For trichomonas, although there was a trend toward PCR detection of more infections in symptomatic males, it was not statistically significant (20% vs. 14.5%; P=.2).
When multipathogen infections were eliminated from the analysis, there was no significant difference in rates of chlamydial infection between symptomatic and asymptomatic men. However, the prevalence of T. vaginalis was significantly higher in the asymptomatic group, compared with men with urethral symptoms (51.4% [18/35] vs. 23% (14/61); P=.009; table 2). None of the 3 pathogens was identified in 67 (43.2 %) of 155 men with urethral symptoms. Of the 107 men with urethral symptoms in whom gonorrhea was not detected—that is, those men with symptoms consistent with the clinical syndrome of NGU—20 (18.7%) had chlamydial infection only, 14 (13.1%) had trichomonas only, and 6 (5.6 %) were infected with both pathogens.
Table 2.
Distribution of symptoms among men infected with a single pathogen (n=96).
Evidence of inflammation on Gram stain, defined as ⩾5 polymorphonuclear leukocytes (PMNs)/oil immersion field (oif), was found in 174 (58%) of 300 subjects. Of these 174 subjects, 49 (28.2%) denied having genitourinary symptoms. Conversely, 49 (33.8%) of 145 asymptomatic patients had inflammation on Gram stain. Of the 174 subjects with ⩾5 PMNs/oif, 105 (60.3%) had 1 of the 3 pathogens detected. Table 3 shows the prevalence of the individual STDs in men with and without urethral inflammation on Gram stain. Infections due to chlamydia and gonorrhea were significantly more likely to be accompanied by inflammation. However, there was no association between the presence of inflammatory cells and infection in men with trichomonas. Infection with T. vaginalis was present in 10.6% of men who lacked evidence of inflammation on urethral Gram stain. Urethritis, as defined by symptoms and/or inflammation, was present in 204 (68%) of 300 men. Of these 204 men, 27%, 26%, and 21% were infected with chlamydia, gonorrhea, and trichomonas, respectively. Among men with NGU (151 [50.3%] of 300), 20.5% had chlamydia only, 15.2% had trichomonas only, and 4.6% had both. Overall, chlamydia was detected in 25.2% of men with NGU, and trichomonas was detected in 19.9%. No evidence of chlamydia or trichomonas was found in 59.6% of men with NGU. Figure 1 depicts a flow chart of patients stratified by the presence of symptoms and/or inflammation on urethral Gram stain, as well as the presence of STDs. Of note, 13 (13.5%) of 96 men without symptoms or inflammation were positive for chlamydia and/or trichomonas. Of the 52 men with trichomonas, 10 (19.2%) lacked symptoms and inflammation on Gram stain.
Table 3.
Relationship of inflammation to sexually transmitted diseases.
Among this group of men attending an urban STD clinic, the prevalence of T. vaginalis infection, as detected by PCR, was similar to the prevalence of gonorrhea and chlamydial infections. Gonorrhea was detected in 17.7%, chlamydia in 19.6%, and trichomonas in 17.3%. Although previous studies of women have documented frequent trichomonas coinfection with gonorrhea or chlamydial infection, our study of men is the first to demonstrate such high T. vaginalis coinfection rates with chlamydial infection and confirms the high coinfection rates with T. vaginalis and N. gonorrhoeae found in 1 previous study [15]. Also noteworthy is our finding that there was no significant difference in the prevalence of trichomonas infection when participants were subset by the presence or absence of genitourinary symptoms. In fact, among those with trichomonas infection alone, significantly more men presented without symptoms. This reservoir of asymptomatic infections in men probably represents an important source of repeated infections in women, accounting for the continued high prevalence of trichomoniasis in women at a time when the prevalence of other treatable STDs in our community is declining [10, 12, 16, 17].
Several factors probably contributed to the large proportion of men with trichomoniasis without symptoms or signs of urethritis. Asymptomatic trichomoniasis is well described in women, particularly when more-sensitive detection methods, such as culture or PCR, are used. Thus, it is not surprising that the same phenomenon is present in men. Furthermore, in the absence of formal current control programs, it is likely that prevalent infections with minimal associated signs or symptoms might accumulate in at-risk populations, as suggested by Wasserheit and Aral [18].
Discussion. Our findings suggest that trichomoniasis may be an important cause of NGU. Nearly 20% of the men in our study with NGU were infected with trichomonas. The etiology of NGU has been carefully studied for >30 years, and all studies confirm that C. trachomatis is a major pathogen that causes this syndrome. For men without chlamydial infection, suggested etiologies of NGU include trichomoniasis, herpes simplex virus, and genital Mycoplasma/ureaplasmas, including M. genitalium. In the 1970s, several carefully conducted studies clearly demonstrated that C. trachomatis was the most common demonstrable pathogen, accounting for 30%–40% of cases of NGU [19–21] in men. However, in a more-recent, large, multicenter study [22], only 15% (range, 4%–35%; in 11 participating centers) of patients with NGU were found to be culture positive for C. trachomatis. Furthermore, more recent studies evaluating the etiology of NGU continue to demonstrate that, in the largest proportion of cases, no pathogen is demonstrable [23]. In addition, although tetracyclines or azithromycin treatment is associated with the resolution of many cases of NGU, cure rates with these drugs for patients without chlamydial infection are lower than those for patients with chlamydial infection [22, 24, 25]. Taken together, these observations suggest that T. vaginalis, as well as other pathogens, such as M. genitalium and herpes simplex virus, which may not respond well to currently recommended therapy, currently may cause many cases of NGU. Comprehensive studies to further study the etiology of NGU, the most common urethritis syndrome in the United States, are needed.
Among this group of men, 43% of those who complained of urethral symptoms had no evidence of gonorrhea, chlamydial infection, or trichomoniasis. Two-thirds of these men also had objective signs of urethral inflammation detected on Gram stain. In addition, 22% of participants who denied symptoms and had none of the 3 pathogens studied present also had objective signs of inflammation, which suggests that these individuals also had asymptomatic NGU. Although we did not test for other organisms thought to be etiologic agents of NGU, the role and potential contribution to the etiology of the clinical findings, which are termed NGU, remains speculative. Thus despite the use of highly sensitive DNA amplification techniques, almost half of all cases of NGU are of unknown etiology.
In summary, among men attending an urban STD clinic, the prevalence of T. vaginalis infection did not differ significantly from the prevalence of gonorrhea or chlamydial infection. Infection with T. vaginalis was present in 19.9% of men with NGU, but also was not associated often with genitourinary signs or symptoms. Coinfection with gonorrhea and trichomonas was nearly as common as coinfection with chlamydia and gonorrhea. Further evaluation of the prevalence and clinical manifestations of T. vaginalis, particularly as the infection relates to NGU, in men are needed. Consideration should be given to including specific treatment for trichomonas as initial treatment for NGU and gonococcal infections.
Acknowledgments
We thank the assistance of Bari Cotton, Ilet Dale, Anna Lee Hughes, and Moira Venglarik, for assistance with patient enrollment, and Heather Hall, for administrative support.
Footnotes
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Financial support: National Institutes of Health (NIH) Sexually Transmitted Disease Cooperative Research Centers (grant AI 38514); NIH Sexually Transmitted Diseases Clinical Trials Unit (grant NO AI 75329).
- Received December 18, 2002.
- Accepted March 5, 2003.
- © 2003 by the Infectious Diseases Society of America
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