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M A J O R A R T I C L E

Added Benet of Nucleic Acid Amplication

Testing for the Diagnosis of Trichomonasvaginalis Among Men and Women Attending a Sexually Transmitted Diseases Clinic

Christina A. Muzny,1 Reaford J. Blackburn,2 Richard J. Sinsky,3 Erika L. Austin,1 and Jane R. Schwebke1

1Division of Infectious Diseases, 2Department of Medicine, University of Alabama at Birmingham, and 3Quality, Improvement, and Decision Support,

Jefferson County Department of Health, Birmingham, Alabama

(See the Editorial Commentary by Taylor on pages 842–4.)

Background . Trichomonas vaginalis (TV) is the most common nonviral sexually transmitted infection (STI) in the

world. However, TV is not a reportable STI and, with the exception of HIV-positive women, there are no guidelines forscreening in women or men. The objective of this study was to determine the added value of nucleic acid amplication

tests (NAATs) for detection of TV in men and women at high risk for infection as well as correlates of infection.

Methods. This was a review of clinical and laboratory data of men and women presenting to the Jefferson County

Department of Health Sexually Transmitted Diseases (STD) Clinic and receiving a TV NAAT.

Results. During 2012–2013, 6335 patients (3821 women and 2514 men) received a TV NAAT on endocervical,

urethral, or urine specimens. Overall TV prevalence was 20.2%; 27.0% in women and 9.8% in men. Correlates of

TV among men included age >40 years, African American race, and ≥5 polymorphonuclear cells per high-power

eld on urethral Gram stain. Age >40 years, African American race, leukorrhea on wet mount, elevated vaginal pH,

positive whiff test, and concurrent gonococcal infection were positively associated with TV among women. TV NAAT

detected approximately one-third more infections among women than wet mount alone.

Conclusions. TV prevalence among men and women was high in this study, suggesting that both groups should be

routinely screened, including those aged >40 years. Improved detection of TV by routine implementation of NAATsshould result in better control of this common, treatable STI.

Keywords. infectiousness; nucleic acid amplication test; sexually transmitted infection; Trichomonas vaginalis;

wet mount.

Trichomonas vaginalis (TV) is the most common non-

viral sexually transmitted infection (STI) [1]. In the

United States, incidence in women of reproductive

age is estimated to be 3–5 million cases annually [2],

and prevalence among women aged 14–49 years in

the general population is 3.1% [3]. Risk factors for TV in

women include older age, African American race, lower

socioeconomic status, and greater numbers of lifetime

sexual partners [3–6]. The epidemiology of TV in

men is less well characterized, as men are not routinely

tested due to a previous lack of sensitive and convenient

testing methodologies. Prior estimates of TV prevalence

in men have ranged from 3% to 20% depending on the

presence or absence of urogenital symptoms, geograph-

ic locale, clinical setting, and method of testing [7–11].

Limited data suggest that risk factors in men include

older age and African American race [8, 12].

Received 3 March 2014; accepted 5 May 2014; electronically published 13 June

2014.

Presented in part: University of Alabama at Birmingham Department of MedicineResearch Day, 5 March 2014. Poster presentation 71. University of Alabama at

Birmingham Health Disparities Research Symposium, 20 March 2014. Oral

presentation.

Correspondence: Christina A. Muzny, MD, Division of Infectious Diseases,

University of Alabama at Birmingham, ZRB 242, 1530 3rd Ave S, Birmingham, AL

35294 ([email protected]).

Clinical Infectious Diseases 2014;59(6):834–41

© The Author 2014. Published by Oxford University Press on behalf of the Infectious

Diseases Society of America. All rights reserved. For Permissions, please e-mail:

[email protected].

DOI: 10.1093/cid/ciu446

834 • CID 2014:59 (15 September) • Muzny et al

mailto:[email protected]:[email protected]:[email protected]:[email protected]


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TV has been shown to be associated with increased suscept-

ibility to human immunodeciency virus (HIV) [13] and ad-

verse pregnancy outcomes [14]. TV is not a reportable STI;

with the exception of HIV-positive women [15], there are no

guidelines for screening in women or men. TV is most fre-

quently diagnosed by examination of a wet mount of vaginal

uid, which has a sensitivity of 50%–60% [16, 17]; wet mount

of urethral secretions in men is less reliable and not routinely

practiced [7]. The gold standard for TV diagnosis in womenhas been culture of vaginal uid, which requires incubation

and is categorized by the Clinical Laboratory Improvement

Amendments (CLIA) as moderately complex [18]; the optimal

site or specimen for diagnosis in men using culture is unknown

[19]. TV culture is not readily available in clinical settings and

sensitivity is less compared to the recently available, highly sen-

sitive nucleic acid amplication test (NAAT) [20]. The TV

NAAT has been validated in asymptomatic and symptomatic

women in multiple specimen types [21, 22] and is run on the

same instrumentation platforms for Chlamydia trachomatis

(CT) and Neisseria gonorrhoeae (GC) testing [21–23]. Although

the TV NAAT can be used to test male urethral and urine spec-

imens, US Food and Drug Administration clearance has not

been sought for this purpose [23].

The Jefferson County Department of Health Sexually Trans-

mitted Diseases (STD) Clinic in Birmingham, Alabama, imple-

mented routine TV NAAT testing on endocervical, urine, and

urethral specimens collected from women and men presenting

to the clinic in March 2012 (women) and November 2012

(men). All women have a wet mount of vaginal uid. Prior to

implementation of NAAT, no TV testing was available for men,

as only Gram staining of urethral discharge is performed. Our

primary objective was to determine the added value of NAATfor TV detection in men and women as well as correlates of in-

fection. We also sought to compare clinical and laboratory char-

acteristics of women that were TV wet mount positive, NAAT

positive with those that were TV wet mount negative, NAAT

positive, as we sought to develop an algorithm for targeted

TV NAAT use in women with a negative wet mount for TV.

METHODS

This study was approved by the Institutional Review Board at the

University of Alabama at Birmingham and by the JeffersonCounty Department of Health. Patients presenting to the STD

Clinic and receiving a TV NAAT between March 2012 and Sep-

tember 2013 were identied from the electronic medical record.

This clinic serves a lower-income, minority (>90% African

American) population; patients are asked to pay $5 to see a clini-

cian and receive STI testing. Inclusion criteria included age ≥16

years and receipt of a TV NAAT on an endocervical or urine

specimen between March 2012 and September 2013 (women)

and on a urethral or urine specimen between November 2012

and September 2013 (men). Only data from the rst clinic visit

per patient during this time frame were reviewed.

Variables abstracted included age, race, circumcision status,

urogenital symptoms, and current clinical diagnoses at the

time of clinic visit: cervicitis, pelvic inammatory disease, bac-

terial vaginosis (BV) (based on Amsel criteria [24]), and vulvo-

vaginal candidiasis. Laboratory variables included vaginal pH,

whiff test (presence of a shy odor when 10% potassium hy-droxide is added to a sample of vaginal discharge), presence

of trichomonads, clue cells (squamous epithelial cells coated

with anaerobic bacteria that have sloughed off from the vaginal

epithelium), and white blood cells (WBCs) per high-power eld

(HPF) on vaginal wet mount (point-of-care test in women),

number of polymorphonuclear cells (PMNs) on urethral

Gram stain per HPF (point-of-care test in men), and TV, CT,

and GC NAAT results on endocervical, urethral, or urine spec-

imens using the Gen-Probe Aptima Combo 2 assay (Gen-

Probe, San Diego, California) (send out test, results take 7

days). It was also noted whether patients with TV were treated

with metronidazole (provided at no additional charge by the

clinic and given on site) at the time of their clinic visit on the

day in which the TV NAAT was obtained, presumably either

due to a positive wet mount for TV (women), clinical diagnosis

of BV (women), or because they were a contact to TV (women

and men). At this clinic, asymptomatic and symptomatic pa-

tients with a positive TV NAAT are asked to return for treat-

ment if they had not already received metronidazole on the

day in which the NAAT was obtained.

Statistical analyses were performed using Stata 12.1 (StataCorp,

College Station, Texas). The association of demographic and clin-

ical characteristics with TV infection was examined separately forwomen and men, with logistic regression used to calculate odds

ratios (ORs) and condence intervals (CIs) in unadjusted and ad-

justed models. All variables of interest were rst examined sepa-

rately in unadjusted models to assess bivariate associations. The

adjusted models include all variables observed to be signicant at

P < .05 in the unadjusted analyses.

RESULTS

Data were available for 6335 patients: 3821 women and 2514

men. The majority were aged 25–

40 years and most (86%)were African American (Table 1). Based on NAAT results, the

overall prevalence of TV was 1279 of 6335 (20.2%); TV preva-

lence by sex was 1032 of 3821 (27.0%) among women and 247

of 2514 (9.8%) among men. TV prevalence by wet mount

among women was 736 of 3765 (19.6%). This was signicantly

lower than the 27.0% prevalence found among women using

NAAT (P < .001), signifying that NAAT detected approximately

one-third more infections among women than wet mount.

Trichomonas vaginalis Molecular Testing • CID 2014:59 (15 September) • 835


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A total of 3765 women had both wet mount and NAAT re-sults available (wet mount results were not available for 56

women). Of these women, 317 had discordant results, including

301 who were TV negative according to wet mount but TV pos-

itive according to NAAT (false-negative wet mounts) and 16

who were TV positive according to wet mount but TV negative

according to NAAT (false-positive wet mounts). A large pro-

portion of women testing positive for TV based on wet

mount (254/736 [34.5%]) (data not shown) and NAAT (375/

1032 [36.3%]) did not complain of urogenital symptoms.

Tables 2 and 3 report correlates of TV among men and

women based on NAAT results. In unadjusted analyses, age(>40 years) and African American race were positively associat-

ed with TV among both groups. Presence of urogenital symp-

toms among men at the time of clinic visit was not associated

with TV; however, women with urogenital symptoms were

more likely to have TV (OR = 1.28 [95% CI, 1.11–1.49]).

Women with a clinical diagnosis of BV or vulvovaginal candi-

diasis were less likely to have TV (OR = 0.69 [95% CI, .58–.82]

and OR = 0.28 [95% CI, .21–.38], respectively). Neither

cervicitis nor pelvic inammatory disease was associated with

TV. Having ≥5 PMNs per HPF on urethral Gram stain (ie, sug-

gestive of a diagnosis of nongonococcal urethritis [NGU]) at the

time of the TV NAAT was positively associated with TV in men

(OR = 2.25 [95% CI, 1.59–3.20]) as was elevated WBCs per HPF

(ie, leukorrhea) on wet mount for women (OR for WBCs 1–

10 = 1.71 [95% CI, 1.39–2.09]; OR for WBCs 11–30 = 2.93

[95% CI, 2.25–3.82]). Elevated vaginal pH ≥4.5 (OR = 1.85

[95% CI, 1.52–2.26]) and positive whiff test (OR = 1.31 [95%CI, 1.13–1.51]) were also positively associated with TV among

women; however, the presence of clue cells on wet mount was

not. Among men, concurrent CT was associated with reduced

likelihood of TV (OR = 0.42 [95% CI, .28–.62]) as was concur-

rent GC (OR = 0.31 [95% CI, .16–.58]). In contrast, concurrent

GC was positively associated with an increased likelihood of TV

among women (OR = 1.62 [95% CI, 1.26–2.08]), although con-

current CT was not. After adjusting for other signicant vari-

ables in each of the models for men and women, all correlates

found to be signicant in unadjusted analyses remained sig-

nicant in adjusted models (Tables 2 and 3) except for the

presence of urogenital symptoms in women, which became

nonsignicant.

The proportion of women that were TV wet mount negative,

NAAT positive was 29.5% (301/1021). Table 4 examines clinical

and laboratory correlates of women with results that were TV

wet mount negative, NAAT positive. In unadjusted analyses,

women with urogenital symptoms (OR = 0.73 [95% CI,

.55–.96]), elevated vaginal pH ≥4.5 (OR = 0.13 [95% CI,

.07–.21]), positive whiff test (OR = 0.70 [95% CI, .54–.93]),

and leukorrhea on wet mount (OR for WBCs 1–10 = 0.37

[95% CI, .25–.55]; OR for WBCs 11–30 = 0.11 [95% CI,

.06–.20]) had lower odds of being TV wet mount negative,NAAT positive. Conversely, women with concurrent GC had

increased odds of having results that were TV wet mount neg-

ative, NAAT positive (OR = 2.08 [95% CI, 1.39–3.13]). After ad-

justing for all signicant correlates in the unadjusted models,

both urogenital symptoms and whiff test positivity failed to

maintain signicance in the adjusted model.

Of those men and women with positive TV NAAT results,

148 of 247 (59.9%) men and 863 of 1032 (83.6%) women

were treated with metronidazole at the time of their initial clinic

visit (data not shown).

DISCUSSION

This is one of the rst studies to report TV prevalence and cor-

relates of infection among men and women attending an STD

clinic in which a TV NAAT was obtained during routine care.

In this relatively large clinic population, TV prevalence (based

on NAAT) was 27.0% in women and 9.8% in men. This prev-

alence in women is signicantly higher than the 3.2% (as

Table 1. Characteristics and Prevalence of Trichomonas vaginalis (TV) Infection Among Patients Undergoing TV NucleicAcid Amplication Testing (N = 6335)

Characteristic

Women

(n = 3821)

TV Prevalence

Among

Women

Men

(n = 2514)

TV Prevalence

Among Men

Age, y

40 618 (16.2) 211 (34.1) 520 (20.7) 84 (16.1)

Race/ethnicitya

AfricanAmerican

3286 (86.0) 957 (29.1) 2159 (85.8) 236 (10.9)

White 439 (11.5) 73 (16.7) 257 (10.2) 10 (3.9)

Hispanic/ Latino

73 (1.9) 1 (1.4) 88 (3.5) 1 (1.1)

Other 23 (0.6) 1 (4.2) 10 (0.4) 0 (0.0)

Overall TV prevalence

TV NAATb 1032 (27.0) 247 (9.8)

Wet mount 736 (19.6) NA

Data are presented as No. (%). Patients were seen at the Jefferson County

Department of Health Sexually Transmitted Diseases Clinic, Birmingham,

Alabama, March 2012 to September 2013.

Abbreviations: NA, not applicable; NAAT, nucleic acid amplification test; TV,

Trichomonas vaginalis .a

Patients reporting Hispanic/Latino ethnicity are included in that category only.

Other race/ethnicity includes American Indian or Alaska Native (n = 5), Asian

(n = 14), Native Hawaiian or other Pacific Islander (n = 4), multiple races

(n = 9), or unreported/refused to answer (n = 21).b Diagnosed by NAAT on urethral or urine specimens for men and endocervical

or urine specimens for women. Overall prevalence of TV infection among all

patients in the sample was 20.2%.



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determined by polymerase chain reaction) reported in the

2001–2004 National Health and Nutrition Examination Survey

(NHANES), the most recent study of TV prevalence in the

United States [25]. It is also higher than in other STD clinic

populations (2%–18%) [26–29], including previous studies per-

formed at this clinic using wet mount [20]. This is likely due to

the improved sensitivity of NAAT compared with other diag-

nostic methods. Using data collected from 15 STD clinics,Meites et al found that TV prevalence (determined by wet

mount, culture, NAAT, or any other type of test) among symp-

tomatic women was 26.2% [30]. TV prevalence among women

in our study (27.0%) was similar but included both sympto-

matic and asymptomatic women. The lower TV prevalence

found among men in our study, compared with women, is likely

inuenced by the high rate (36%–69%) of spontaneous resolu-

tion of TV that is known to occur in men [19, 31]. Prevalence of

TV based on wet mount among women was 19.6%, suggesting

that TV would have gone undiagnosed in approximately one-

third of infected women had NAAT not been performed.Correlates of TV among men and women based on NAAT

included age (>40 years) and African American race, similar

to previous studies [3–5, 8, 12]. Unlike CT and GC [32], older

age is a signicant risk factor for TV in men and women [4],

perhaps due to accumulating infections caused by lack of detec-

tion. Potential reasons for the racial disparity have been previ-

ously discussed [5], although the fact that the majority of

patients seen in our clinic are of African American race may

have also inuenced this nding. Among men, having ≥5

PMNs per HPF (suggestive of NGU) on urethral Gram stain

was also correlated with TV; TV is known to be an important

cause of NGU [19]. Additional correlates of TV among women

included leukorrhea on wet mount, similar to that noted by Laz-

enby et al [33], elevated vaginal pH (TV prefers a high pH for

optimal growth) [18], positive whiff test, and concurrent gono-

coccal infection. Among men and women with a positive TVNAAT, 40.1% of men and 16.4% of women had not been treated

with metronidazole at the time of their initial clinic visit, signi-

fying missed opportunities for treatment.

It is noteworthy that the presence of urogenital symptoms

among men and women was not correlated with TV. This is

consistent with the ndings of Nye et al, which showed that

no symptoms were specic for any positive TV test [20]. In ad-

dition, similar to others [20], the results of our study suggest

that TV can often be a subclinical infection, as approximately

one-third of women with TV-positive results based on wet

mount and one-third of women with TV-positive resultsbased on NAAT did not complain of urogenital symptoms at

the time of their clinic visit.

We also found that TV was not associated with BV among

women. It has been suggested that TV may alter the vaginal mi-

crobiota in a manner that is favorable to its survival and trans-

missibility [34]. Hillier et al found that pregnant women with

intermediate Nugent scores [35] had the highest prevalence of

TV [36]. Martin et al corroborated this nding in a subset of 394

Table 2. Correlates of Trichomonas vaginalis (TV) Infection Among Men Undergoing TV Nucleic Acid Amplication Testing (n = 2514)

Characteristic

TV Negative

(n = 2267)

TV Positivea

(n= 247)

Unadjusted OR

(95% CI) P Value

Adjusted OR

(95% CI) P Value

Age, y


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nonpregnant women [34] whereas Brotman et al have shown

that intermediate vaginal ora or BV (based on Nugent score)

at a prior visit is associated with 1.5- to 2-fold increased risk for

incident TV among a cohort of 3620 nonpregnant women [37].

In vitro data suggest that TV grows better in an elevated pH

[38]; BV can provide this high-pH environment. TV itself

may also be able to manipulate the vaginal environment and

promote changes in the vaginal ora, leading to an elevated

pH. Indeed, the majority of women (82.9%) testing positivefor TV (based on NAAT) in our study had an elevated vaginal

pH (Table 3). Although a clinical diagnosis of BV was not cor-

related with TV, it would have been of interest to look at the dis-

tribution of Nugent scores among women testing TV positive to

see if they were in the abnormal range. However, we did not

have these data available.

An unexpected nding was that concurrent CT and GC

were associated with reduced likelihood of TV among men.

Explanations for this are unknown, although it could be related

to cumulative asymptomatic infection caused by TV in men as

opposed to symptomatic infection with CT or GC whereby men

would actively seek care at an STD clinic. Indeed, only 72 of 247

(29.1%) of men in this study positive for TV by NAAT had

complaints of urogenital symptoms (Table 2). Unfortunately,

we did not have the data available to know whether or not

men testing positive for TV reported being a contact to TV

upon presenting to the clinic; however, the fact that 59.5%were treated with metronidazole at the time of their visit

strongly suggests this. Conversely, concurrent GC was positively

associated with increased likelihood of TV among women. It

has been reported that TV is associated with GC in women

8%–50% of the time and that GC prevalence is 1.4–1.9 times

higher in women with TV than in women without TV [39].

This correlation between TV and GC has also been noted by

Lossick in a study of 3507 TV cases [40] and Lazenby et al in

Table 3. Correlates of Trichomonas vaginalis (TV) Infection Among Women Undergoing TV Nucleic Acid Amplication Testing (n = 3821)

Characteristic

TV Negative

(n = 2789)

TV Positivea

(n = 1032)

Unadjusted OR

(95% CI) P Value

Adjusted OR

(95% CI) P Value

Age, y


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a study of 294 women, of whom 16% had TV [ 33]. Similar toour results, a correlation between TV and CT has not been

noted in prior studies [40]. The biologic and/or social differenc-

es that account for these ndings are unknown. It could be hy-

pothesized that the demographic pool of CT infections among

women may be more diffuse than the pool of TV/GC infections

and that risk factors for acquiring CT are different than those

for acquiring TV/GC [40].

We originally hypothesized that women with TV wet mount–

negative, NAAT-positive results would have a lower burden of

disease due to TV and be less likely to have urogenital symptoms,

elevated vaginal pH, and leukorrhea on wet mount than womenwith TV wet mount–positive, NAAT-positive results. The results

of our study are somewhat consistent with this as women with an

elevated vaginal pH and leukorrhea had lower odds of having re-

sults that were TV wet mount negative, NAAT positive. Women

with urogenital symptoms initially also had a lower odds of hav-

ing TV wet mount–negative, NAAT-positive results, although

this nding lost its signicance in adjusted analysis. Only concur-

rent gonococcal infection was found to be signicantly correlated

with TV wet mount negativity, NAAT positivity. The biologicbasis for this unexpected nding is unknown. In terms of algo-

rithmic testing, the results of our study suggest that patients

with an elevated pH and leukorrhea on wet mount should be

evaluated with a more sensitive TV diagnostic test, preferably

NAAT, particularly if microscopy is negative for TV. Clearly,

all STD clinic clients should be screened for TV and reex testing

in general; that is, NAATs (particularly if wet mount is negative),

could be used as a cost-saving measure.

Our study has several limitations. First, data were collected

retrospectively, limiting the amount of sexual history (including

reason for clinic visit), clinical diagnosis, and laboratory data(including HIV testing results) able to be extracted. Because

of this, there may be additional correlates of TV not identied

here. Second, the results of this study were obtained from one

STD clinic in the southern United States and may not be gen-

eralizable to other clinical settings. Additionally, as only data

from the rst clinic visit per patient during the study time

frame was reviewed, we were unable to determine whether

men and women with TV had a new infection vs a persistent

Table 4. Comparison of Wet Mount Positivity/Negativity With Positive Nucleic Acid Amplication Test for Trichomonas vaginalis (n = 1021 Women Positive)a

Characteristic

TV Wet Mount−

(n= 301)

TV Wet Mount+

(n= 720)

TV-, Wet Mount/TV+

NAAT, Unadjusted

OR (95% CI) P Value

TV- Wet Mount/TV+

NAAT, Adjusted

OR (95% CI) P Value

Urogenital symptomsb 176 (58.5) 473 (65.7) 0.73 (.55–.96) .03 1.00 (.72–1.38) .98

Current laboratory diagnosis

Vaginal pHc


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or recurrent infection. Because of this, we were also unable to

determine the exact percentage of patients with a positive TV

NAAT who received treatment with metronidazole as we only

had data available from the clinic visit on the day in which

the NAAT was obtained.

Nevertheless, this study demonstrates that routine imple-

mentation of TV NAAT at our STD clinic was able to detect

a signicant proportion of infected male and female patients,

signicantly higher than that detected by wet mount alone inwomen. The TV NAAT can easily be implemented in clinical

settings as it can be run on the same instrumentation platforms

available for CT and GC testing. Improved detection of TV by

implementation of NAAT in men and women of all age groups

should be considered, as it will likely result in better control of

this common, treatable STI.

Notes

Acknowledgm ents. The authors thank Edwin Swiatlo, MD, PhD, for

helpful discussions on manuscript preparation.

Financial support. C. A. M. is supported in part by a developmental

grant from the American Sexually Transmitted Diseases Association.

Potential con icts of interest. J. R. S. has been a consultant for and re-

ceived research support from Hologic/GenProbe, BD Diagnostics, Cepheid,

and Embil Pharmaceuticals. All other authors report no potential conicts.

All authors have submitted the ICMJE Form for Disclosure of Potential

Conicts of Interest. Conicts that the editors consider relevant to the con-

tent of the manuscript have been disclosed.

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