Correlation of Leukorrhea and Trichomonas vaginalis Infection

Gweneth B. Lazenby,a David E. Soper,a Frederick S. Nolteb

Department of Obstetrics and Gynecologya and Department of Pathology and Laboratory Medicine,b Medical University of South Carolina, Charleston, South Carolina,
USA

Trichomonas vaginalis is a common sexually transmitted infection (STI) causing vaginitis. Microscopy has poor sensitivity but is
used for diagnosis of trichomoniasis in resource-poor settings. We aimed to provide a more reliable diagnosis of trichomoniasis
by investigating an association with leukorrhea. Women presenting for evaluation of vaginal discharge, STI exposure, or preven-
tative gynecologic examination were evaluated for Trichomonas infection. Vaginal pH was determined and microscopy was per-
formed by the provider, who recorded the number of polymorphonuclear leukocytes (PMNLs) per epithelial cell and the pres-
ence of clue cells, yeast, and/or motile trichomonads. Leukorrhea was defined as greater than one PMNL per epithelial cell.
Culture and a nucleic acid amplification test (NAAT) were used to detect T. vaginalis. Patients were evaluated for Chlamydia
trachomatis and Neisseria gonorrhoeae using NAATs and bacterial vaginosis using Gram stains. Two hundred ninety-four
women were enrolled, and 16% were found to have Trichomonas (46/294). Trichomonas infection was more common in parous
non-Hispanic, black women, who reported low rates of contraceptive use (33% versus 17%; P 0.02) and a STI history (85%
versus 55%; P 0.002). These women were more likely to report vaginal discharge (76% versus 59%; P 0.02) and have an ele-
vated vaginal pH (87% versus 48%; P < 0.001) and gonorrhea infection (15% versus 4%; P 0.002). Leukorrhea was associated
with a 4-fold-increased risk of Trichomonas infection. Leukorrhea on microscopy was associated with Trichomonas vaginitis.
Patients with leukorrhea should be evaluated with more-sensitive tests for T. vaginalis, preferably NAATs, if microscopy is
negative.

T he prevalence of trichomoniasis in U.S. women is more than

the combined prevalences of Neisseria gonorrhoeae and Chla-
mydia trachomatis infections (1). Infection with Trichomonas is
associated with a significant risk of morbidity in women, includ-
ing pelvic inflammatory disease, adverse pregnancy outcomes
(e.g., preterm labor and delivery), cervical dysplasia, infertility,
increased risk of postoperative infection, and HIV acquisition and
transmission (25). U.S. health care costs related to trichomonia-
sis approach 34 million dollars per year (1).
Trichomonas vaginalis is a parasitic flagellate that adheres to
and engulfs vaginal epithelial cells through phagocytosis. The re-
sulting death of epithelial cells leads to inflammation within the
genital tract and an increased number of polymorphonuclear leu-
kocytes (PMNLs) in vaginal fluid (6). An increase in PMNLs
noted on microscopy of vaginal secretions indicates an infectious
or inflammatory process and may be a useful screening tool when
evaluating vaginal discharge.
Leukorrhea refers to the presence of PMNLs in vaginal fluid,
which can be quantified as the number of PMNLs seen on micros-
copy. Previous studies have defined leukorrhea based on the num-
ber of PMNLs per high-power field (hpf). Leukorrhea is consid-
ered present if there are more than one PMNL per oil immersion
field (1,000) or more than 10 PMNLs per hpf (400) (7, 8).
Leukorrhea has also been described according to the ratio of
PMNLs to vaginal epithelial cells; more than 1 PMNL per epithe-
lial cell is consistent with leukorrhea (9).
Noninfectious conditions, such as pregnancy, menstruation,
or infertility, are associated with an increased number of PMNLs
in vaginal fluid (1012). Genital tract infections, such as C. tracho-
matis cervicitis and endometritis, are strongly associated with leu-
korrhea (8). This association of leukorrhea and C. trachomatis
infection is true in pregnant and nonpregnant women. Leukor-
rhea is a strong predictor for C. trachomatis infection in nonpreg-
nant and pregnant women (relative risk [RR], 59; 95% confidence
interval [CI], 8 to 413; versus RR, 16; 95% CI, 7 to 32) (7). The
absence of leukorrhea has a high negative predictive value (95%) for
the diagnosis of upper genital tract infection, i.e., endometritis (8).
There are currently no studies in the English literature for
which a correlation between leukorrhea in vaginal secretions and
Trichomonas infection is reported. This information would be
clinically useful when evaluating vaginal discharge and lower gen-
ital tract symptoms. Microscopy is the most common method
used to diagnose trichomoniasis, but the sensitivity is poor (55%;
35 to 77%) (1316). The presence of leukorrhea in the absence of
motile trichomonads could potentially be presumed to be cervici-
tis and empirically treated without further evaluation for
Trichomonas. A known significant relationship between leukor-
rhea on microscopy and Trichomonas might prompt clinicians to
screen women in this clinical scenario for this common infection
using more-sensitive methods.
The objective of this study was to determine an association
between the presence of leukorrhea on microscopy of vaginal se-
cretions and Trichomonas infection.
MATERIALS AND METHODS
The study was approved by the Medical University of South Carolina
Institutional Review Board (HR no. 19180). Two hundred ninety-four
Received 12 February 2013 Returned for modification 6 March 2013
Accepted 5 May 2013
Published ahead of print 15 May 2013
Address correspondence to Gweneth B. Lazenby, lazenbgb@musc.edu.
Copyright 2013, American Society for Microbiology. All Rights Reserved.
doi:10.1128/JCM.00416-13

July 2013 Volume 51 Number 7 Journal of Clinical Microbiology p. 23232327 jcm.asm.org 2323
Lazenby et al.

women presenting to our urban academic practice for a gynecologic TABLE 1 Patient characteristics
exam were enrolled in the study. Patients were eligible for the study if Characteristica Value
they had undergone an Aptima Combo 2 assay for N. gonorrhoeae and
Age (yr) (mean SD) 28 9
C. trachomatis (Gen-Probe Inc., San Diego, CA) as part of a routine
Parity, median (interquartile range) 1.4 (08)
exam or an evaluation for vaginal discharge or sexually transmitted
infection (STI) exposure. Women were excluded if they were preg- % of patients (no. of patients/total) with characteristic
nant, HIV positive, and/or had a gynecologic malignancy, vaginal Non-Hispanic, black race 74 (216/293)
bleeding, or an active genital herpes infection. Women were also ex- Hispanic race 0.6 (2/293)
cluded if they had undergone surgery or were treated for pelvic inflam- Single marital status 90 (260/290)
matory disease, appendicitis, vaginitis, or a STI within 28 days of pre- Exclusively heterosexual partner preference 98 (287/292)
sentation. The following patient information was collected: age, race, Vaginal douching 16 (46/286)
marital status, parity, first day of last menstrual period, contraceptive Regular menstrual cyclesb 63 (170/272)
use, condom use, douching practices, partner gender preference, num- Currently not using contraception (including condoms) 20 (58/292)
ber of partners in the last year, history of STIs, and history of abnormal Report condoms only for contraception 7 (22/294)
cervical cytology. Hormonal contraception 58 (169/292)
During a gynecologic examination, the following tests were per- Surgical contraceptionc 14 (41/292)
formed: vaginal pH, Gram stain, T. vaginalis culture (InPouch, Biomed History of abnormal cervical cytology 17 (47/275)
diagnostics, White City, OR), nucleic acid amplification tests (NAATs) for Multiple sexual partnersd 24 (68/278)
N. gonorrhoeae, C. trachomatis, and T. vaginalis (Aptima Combo 2 and TV Patient reported vaginal discharge 61 (179/292)
analyte specific reagent; Gen-Probe Inc., San Diego, CA), and microscopy History of one prior sexually transmitted infection (STI) 60 (175/292)
of vaginal secretions. The microscopy specimen was prepared by placing a History of more than one STI 49 (84/170)
History of Trichomonas infection 40 (66/170)
vaginal swab into a test tube containing a small amount of normal saline
History of Chlamydia infection 62 (106/170)
(approximately 3 drops). A drop of this solution was then placed on a glass
History of gonorrhea infection 37 (61/166)
slide and reviewed under an hpf (400). When reviewing microscopy of
History of genital herpes 12 (21/170)
vaginal secretions, examiners noted the presence of PMNLs, clue cells, a
Some patient characteristic data were not available for all participants.
yeast, and/or motile trichomonads. Leukorrhea on microscopy was de- b
Regular menstrual cycles defined as monthly menses every 21 to 35 days.
fined as 1 PMNL per epithelial cell per hpf (400). Clinicians perform- c
Surgical contraception may include female tubal ligation or male vasectomy.
ing microscopy were Clinical Laboratory Improvement Amendments d
Defined as 1 partner in the 12 months preceding evaluation.
(CLIA) certified and participated in competency assessment and profi-
ciency testing with guidance from the clinical laboratories point-of-care
testing team. RESULTS
Gram staining of vaginal secretions, T. vaginalis cultures, and NAATs
Two hundred ninety-four women, ages 16 to 67, were enrolled in
were performed by the Medical University of South Carolina Microbiol-
ogy and Molecular Pathology labs. Gram stains were interpreted using
this study. More than 60 percent of the subjects presented for
Nugents criteria to diagnose bacterial vaginosis (BV) (17). The number of evaluation of a vaginal discharge (179). The majority of subjects
PMNLs per hpf on Gram staining was rated using the following scale: 0 were non-Hispanic, black (216) and currently unmarried (260).
PMNLs/hpf, 1 to 5 PMNLs/hpf, and more than 5 PMNLs/hpf. T. vaginalis Ninety-eight percent of women reported being exclusively hetero-
cultures were incubated at 37C and inspected every other day up to 5 days sexual (287), and more than half had a history of an STI (175).
for the presence of motile trichomonads. Most women reported using a method of contraception, includ-
Vaginal swab samples were transported to the laboratory for NAATs ing condoms (234). Other patient characteristics are listed in
using the Aptima transport medium. The Aptima Combo 2 assays for N. Table 1.
gonorrhoeae and C. trachomatis were performed and interpreted accord- Trichomonas testing results were available for almost all 294
ing to the manufacturers recommendations using the semiautomated women enrolled in the study: 292 T. vaginalis cultures and 247
direct tube sampling (DTS) system. The Aptima T. vaginalis analytic- nucleic acid amplification tests. Sixteen percent (46) of the study
specific reagent was used to develop a NAAT for T. vaginalis on the DTS subjects had a positive Trichomonas test result. Women with a
system (4). Aliquots of the Aptima vaginal swab transport medium were Trichomonas infection were more likely to be parous (88% versus
stored for up to 12 months at 70C before testing for T. vaginalis. Spec- 64%; P 0.002) and non-Hispanic black (93% versus 70%; P
imens with relative-light-unit values of 100,000 were considered nega- 0.0004). They were less likely to use any form of contraception
tive, and those with 100,000 relative-light-unit values were considered (33% versus 17%; P 0.02), but rates of condom use were similar
positive. in the two groups (4% versus 8%; P 0.5). Women with
Statistical analyses were performed using the SAS 9.3 software pro-
Trichomonas infection were more likely to report a history of STIs
gram (SAS, Cary, NC). Continuous variables (age and parity) were ana-
(85% versus 55%; P 0.002) (Table 2).
lyzed using Students t test to compare means and the Wilcoxon rank sum
According to Nugents criteria, 41% of women in the study had
test to compare medians. For dichotomous variables, chi-square and Fish-
ers exact tests were used to compare women with and without Trichomo-
BV (119/289). Five Gram stains could not be scored due to inad-
nas infection. Univariate logistic regression analyses were used to deter- equate specimen collection. The rates of BV determined by Nu-
mine factors associated with Trichomonas infection. Variables with a P gents criteria and high-power microscopy findings of clue cells
value of 0.2 were included in multivariate logistic regression analyses. were equal (both 41%), but the agreement between these tests was
Kappa statistics were calculated to determine the agreement between low (kappa statistic 0.5). The rates of BV were similar among
Trichomonas culture and NAATs. Chi-square tests were used to calculate the women infected with Trichomonas versus those not infected
the sensitivity, specificity, and positive and negative predictive values of (43% versus 41%; P 0.7). PMNLs were noted on 71% of all
culture, visualization of motile trichomonads, and leukorrhea on micros- Gram stain specimens. Compared to uninfected women, women
copy for the diagnosis of trichomoniasis. with T. vaginalis were more likely to have PMNLs on Gram stain-

2324 jcm.asm.org Journal of Clinical Microbiology

 Leukorrhea and Trichomonas vaginalis Infection

TABLE 2 Comparison of women with Trichomonas infection and those not infected
Value for groupa
Characteristic Trichomonas infection No Trichomonas P valuee
Age (yr), mean ( SD) 29.3 (10.8) 27.7 (8.6) 0.34
Parity, median (interquartile range) 2 (06) 1 (08) 0.001

% with characteristic (no. of women/total)

Non-Hispanic, black race 93 (43/46) 70 (173/247) 0.0004
Single marital status 91 (41/45) 89 (219/245) 0.7
Exclusively heterosexual 98 (45/46) 98 (242/246) 0.8
Douching 20 (9/45) 15 (37/241) 0.4
Regular menstrual cycles 49 (19/39) 65 (151/233) 0.06
No contraception, including condoms 33 (15/46) 17 (43/246) 0.02
Reported condom use 4 (2/46) 8 (20/248) 0.5*
History of abnormal cervical cytology 15 (7/46) 17 (40/229) 0.7
Multiple sexual partners 26 (11/42) 24 (57/236) 0.7
History of at least one STI 85 (39/46) 55 (136/246) 0.002
Reported vaginal discharge 76 (35/46) 59 (144/246) 0.02
Abnormal vaginal pHb 87 (40/46) 48 (120/248) 0.0001
PMNLs on microscopy 78 (36/46) 49 (118/240) 0.0003
PMNLs on Gram staining 87 (40/46) 69 (167/243) 0.01
Bacterial vaginosisc 43 (20/46) 41 (99/243) 0.7
Chlamydia infectiond 7 (3/46) 4 (11/248) 0.5*
Gonorrhea infection 15 (7/46) 4 (9/248) 0.002
a
For the Trichomonas-infected group, n 46; for the uninfected group, n 253.
b
Abnormal vaginal pH is defined as a pH of 4.5.
c
Bacterial vaginosis is defined as a Nugent score of 7 (17).
d
Determination of Chlamydia and gonorrhea infection was based on positive NAATs.
e
, result of Fishers exact test for small sample size. Otherwise, P values were calculated using chi-square tests.

ing and leukorrhea (1 PMNL per hpf) noted on microscopy The visualization of any PMNLs on Gram staining (hpf, 1,000)
(87% versus 69%; P 0.01; and 78% versus 49%; P 0.0003). was a more-sensitive test for Trichomonas infection than leukor-
Women with Trichomonas were 3 times as likely to have gonor- rhea on microscopy (hpf, 400) (90% versus 78%). However, the
rhea (15% versus 4%; P 0.002), but the rates of C. trachomatis specificity of Gram staining was lower than that of leukorrhea on
infection were not different between groups (7% versus 4%; P microscopy. The PPV for leukorrhea assessed by Gram staining
0.5) (Table 2). versus the PPV for assessment by microscopy were similar, 21 and
Factors associated with Trichomonas infection in univariate lo- 25%, respectively (Table 4).
gistic regression analysis were parity, race, lack of contraceptive
use, history of STIs, vaginal discharge on presentation, an elevated DISCUSSION
vaginal pH (4.5), leukorrhea, and concurrent gonorrhea. When The incidence of Trichomonas vaginalis infection among the
controlling for race and parity, both a history of STIs (odds ratio women in this study population (16%) is five times higher than
[OR], 3.1; 95% CI, 1.3 to 7.4) and lack of contraceptive use (OR,
2.2; 95% CI, 1.1 to 4.7) were associated with Trichomonas infec-
tion. When controlling for abnormal vaginal pH, leukorrhea on
TABLE 3 Factors associated with Trichomonas vaginalis infection
microscopy, and patient-reported vaginal discharge at presenta-
tion, women with a gonorrhea infection were 4 times more likely Regression value (95% CI)
to have trichomoniasis (OR, 3.6; 95% CI, 1.1 to 11.6) (Table 3). Characteristic Univariate Multivariatea
NAATs and T. vaginalis culture were highly correlated (kappa Parous 3.8 (1.69.3) 2.2 (0.85.8)*
statistic 95%). NAATs detected an additional 3 cases of Non-Hispanic, black race 6.1 (1.820.4) 3.0 (0.811.2)*
Trichomonas infection. Compared to NAATs, the sensitivity and Not currently using contraception 2.3 (1.14.6) 2.2 (1.14.7)*
specificity of culture were 93% and 100%. Using NAATs as the History of at least one STI 4.5 (1.910.5) 3.1 (1.37.4)*
gold standard for the diagnosis of Trichomonas infection, the sen- Reported vaginal discharge 2.3 (1.14.6) 1.5 (0.73.2)
sitivity of motile trichomonads on microscopy was very poor Abnormal vaginal pHb 7.1 (2.917.4) 6.0 (2.415.1)
(51%). Leukorrhea (1 PMNL per epithelial cell) on microscopy PMNLs on microscopy 3.7 (1.87.8) 1.8 (0.84.2)
had an increased sensitivity for Trichomonas infection compared PMNLs on Gram staining 3.2 (1.37.8) 2.7 (1.06.7)
Gonorrhea infection 4.8 (1.713.5) 3.6 (1.111.6)
to visualization of motile trichomonads (78% versus 51%), but
the specificity and positive predictive values (PPV) were poor.
a
, multivariate logistic regression model controlling for patient characteristics
associated with Trichomonas infection: parity, race, contraceptive use, and history of
When combining the findings of motile trichomonads and/or leu- STIs. The remaining variables were used in a separate multivariate logistic regression
korrhea on microscopy compared to leukorrhea on microscopy model to determine clinical findings associated with Trichomonas infection.
alone, the sensitivity for diagnosis of Trichomonas was unchanged. b
Abnormal vaginal pH as defined by a pH of 4.5.

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Lazenby et al.
TABLE 4 Diagnostic techniques for the detection of Trichomonas compared to nucleic acid amplification testsa
Method or target % Sensitivity
b
Culture 93 (38/41)
Motile trichomonads 51 (21/41)
Leukorrhea on microscopyc 78 (32/41)
Motile trichomonads or leukorrhea 78 (32/41)
PMNLs on Gram stainingd 90 (37/41)
a
Parenthetical numbers are no. of correct results/no. tested. PPV, positive predictive value; NPV, negative predictive value.
b
InPouch Trichomonas culture was more sensitive and specific than microscopy for the diagnosis of Trichomonas.
c
Leukorrhea, 1 PMNL per epithelial cell per hpf (400).
d
PMNLs on Gram staining, 1 PMNL per hpf (1,000).
the reported prevalence of Trichomonas infection in American
women (1). In our population, Trichomonas vaginitis was associ-
ated with leukorrhea on microscopy (1 PMNL per epithelial cell
per hpf, 400) and PMNLs on Gram staining (1 PMNL per
hpf, 1,000). Both of these findings have lower sensitivity for
Trichomonas infection than for culture (93% versus 78% and
90%, respectively) but improved sensitivity over that for motile
trichomonads on microscopy (51%). Negative predictive values
for motile trichomonads, leukorrhea, PMNLs on Gram staining,
and culture were comparable. In comparison to NAATs for the
diagnosis of trichomoniasis, neither leukorrhea on microscopy
nor Gram staining was specific, and both had low positive predic-
tive values (Table 4).
The incidence of Trichomonas infection in this group of
women is likely not reflective of the general population. Our ob-
stetrics-gynecology (OBGYN) residency womens health practice
provides care to mostly young, minority women with a high rate
of STIs. The mean age of these study subjects was 28 (9) years,
the majority of women (74%) were non-Hispanic black, and more
than half (60%) reported a history of at least one STI (Table 1).
In a national survey of American women, low level of educa-
tion (high school or less), poverty, increasing number of sexual
partners, early age of first sexual intercourse, and douching were
associated with Trichomonas infection (1). In our population,
douching and reporting more than one sexual partner in the past
12 months was not associated with trichomoniasis. These findings
are likely due to the high proportion of patients reporting douch-
ing and multiple partners in the overall study group. Risk factors
associated with Trichomonas infection among the women in this
study were parity, non-Hispanic black race, lack of contraceptive
use, including condoms, and a history of a STI. These factors
associated with increased risk of STIs are consistent with those in
previous reports with the exception of an increased number of
sexual partners (Table 2) (18).
Exam findings associated with Trichomonas vaginitis in our
population were an elevated vaginal pH (4.5), leukorrhea on
microscopy, PMNLs on Gram staining, and gonorrhea infection.
Patient report of vaginal discharge was associated with trichomo-
niasis in univariate analysis, but this association was attenuated in
multivariate analysis when accounting for other exam findings:
pH, PMNLs on Gram staining, and cervicitis (Table 3). The poor
association between symptomatic vaginal discharge is consistent
with other population-based studies of Trichomonas infection (1).
The high rate of asymptomatic infections in women supports the
notion that clinicians should not limit evaluations for Trichomo-
nas vaginitis to microscopy in those reporting vaginal discharge
(19). We suggest that clinicians consider the factors associated
2326 jcm.asm.org
% Specificity % PPV % NPV
100 (205/205) 100 (38/38) 99 (205/208)
98 (200/204) 84 (21/25) 91 (200/220)
51 (102/199) 25 (32/129) 92 (102/111)
53 (109/207) 25 (32/130) 92 (109/118)
33 (68/207) 21 (37/176) 94 (68/72)
with Trichomonas infection in order to identify patients at risk and
use tests more sensitive than microscopy, such as culture or
NAATs, to diagnose Trichomonas infection.
Similar to studies of other genital tract infections, leukorrhea
in vaginal secretions was associated with Trichomonas infection.
This is physiologically plausible, because Trichomonas causes in-
creased inflammation within the vaginal environment and has
been found to attract PMNLs (6). Specifically, CD4 lympho-
cytes are recruited to the site of Trichomonas infection (20).
In the absence of leukorrhea on microscopy (1 PMNL per
epithelial cell), Trichomonas infection was unlikely (OR, 0.3; 95%
CI, 0.1 to 0.8). Although gonorrhea cervicitis was associated with
an increased risk of Trichomonas infection, this did not impact the
association between leukorrhea and Trichomonas vaginitis. When
controlling for the presence of gonorrhea, C. trachomatis infection,
and bacterial vaginosis, patients were 4 times more likely to have
Trichomonas if leukorrhea was noted on microscopy (OR, 3.6;
95% CI, 1.6 to 7.6). Our findings suggest that the presence of
leukorrhea on microscopy should increase clinicians suspicion of
Trichomonas infection and lead to further evaluation with more-
sensitive tests if microscopy is negative for motile trichomonads.
The Aptima T. vaginalis analyte-specific reagent used in this
study has emerged as the most sensitive test for detection of
Trichomonas infections (4, 2123). Because concomitant C. tra-
chomatis and N. gonorrhoeae infections are common in patients
with trichomoniasis, a panel of NAATs for these three infectious
agents would be ideal for comprehensive STI diagnosis. The Ap-
tima T. vaginalis assay was recently cleared by the FDA for diag-
nostic use. This should greatly increase availability of the test, with
cost and turnaround time for results similar to those of the Aptima
C. trachomatis and N. gonorrhoeae assay.
The association between leukorrhea and Trichomonas vaginitis
in our population is both physiologically plausible and likely ap-
plicable to other populations seeking evaluation for vaginal dis-
charge or gynecologic exam. Our study subjects are not represen-
tative of a general population given the young age of participants,
high rates of reported and concurrent STIs, and disproportionate
representation of minorities. However, this population is similar
to others studied in urban centers, STI clinics, and family planning
centers. It is in these low-resource settings that microscopy is often
used for the diagnosis of Trichomonas. Our findings suggest that
the presence of leukorrhea on microscopy should increase clinical
suspicion for Trichomonas vaginitis, prompting additional tests,
and may enhance identification of this common and morbid in-
fection.
Journal of Clinical Microbiology

ACKNOWLEDGMENTS
We acknowledge Gen-Probe, Inc., for their support and funding of this
research.
We thank the staff of the MUSC Microbiology and Molecular Pathol-
ogy labs for their tireless work in analyzing the additional specimens re-
quired for this study. We especially recognize April Kegl.
The coinvestigator Fredrick Nolte has been a member of the Gen-
Probe Scientific Advisory Board from 2007 to the present. The annual
compensation associated with this activity is approximately $10,000. Gen-
Probe products were used to determine the Chlamydia trachomatis, Neis-
seria gonorrhoeae, and Trichomonas vaginalis infection status of the pa-
tients described in our article.
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