Prevalence and risk factors of Ureplasma urealyticum and Mycoplasma genitalium among women with secondary infertility in Vietnam – A crosssectional study
16
MedPharmRes, 2020, 4
MedPharmRes
journal of University of Medicine and Pharmacy at Ho Chi Minh City
Clinical Article
Prevalence and risk factors of Ureplasma urealyticum and Mycoplasma
genitalium among women with secondary infertility in Vietnam – A cross-
sectional study
Tam Minh Leab*, Do Quang Leb, Huy Vu Quoc Nguyenb, Tram Viet Quynh Ngoc, Bach Hoang Nguyenc
aCenter for Reproductive Endocrinology and Infertility, Hue University Hospital, Hue University, Hue City, Vietnam;
bDepartment of Obstetrics and Gynecology, Hue University of Medicine and Pharmacy, Hue University, Hue City,
Vietnam;
cDepartment of Microbiology, Hue University of Medicine and Pharmacy, Hue University, Hue City, Vietnam.
Received December 27, 2019: Revised February 10, 2020: Accepted April 20, 2020
Abstract: Introduction: Ureaplasma urealyticum and Mycoplasma genitalium are infectious pathogens
resulting in non-gonococcal urethritis and complications such as pelvic inflammatory disease (PID) and
infertility. This study aimed to determine the prevalence of U. urealyticum and M. genitalium in women with
secondary infertility and the related factors to these infections. Methods: This cross-sectional descriptive study
was carried out from July 2017 to June 2018. Cervical specimens were collected from women with secondary
infertility at the Center for Reproductive Endocrinology and Infertility, Hue University Hospital, Vietnam. PCR
was applied for detection of U. urealyticum and M. genitalium. Tubal patency was assessed by
hysterosalpingography. Results: Prevalence of U. urealyticum and M. genitalium were 37.9% and 2.1%,
respectively. The association was not statistically significant among infection and the following factors like
age, educational level, occupation, history of miscarriage, history of genital infection and abdominal surgery,
or infertility duration (p > 0.05). There was a statistically significant correlation between U. urealyticum
infection and tubal damage according to hysterosalpingography (p < 0.05). Conclusion: In the case of women
with secondary infertility, genital infection with M. genitalium was rare, whereas that with U. urealyticum
infection was high and appeared to be associated with tubal damage.
Keywords: Ureaplasma urealyticum; Mycoplasma genitalium; infertility; tubal disorder; hysterosalpingography.
1. INTRODUCTION
uterine or peritoneal diseases are most common, whereas tubal
disorder is the second common causes of secondary infertility
in women [3].
Secondary infertility is defined as unable to get a clinical
pregnancy after one year of unprotected sexual intercourse in
couples with a history of at least one pregnancy, birth,
miscarriage, planned abortion, or ectopic pregnancy [1].
Infertility impacts on financial burden on patients and the
health care system as well as in psychological aspect for
millions of couples [2]. Among the major causes of female
infertility, endocrine or ovulatory dysfunction together with
Pelvic inflammatory disease (PID) is one of the most
important causes of tubal disorder leading to infertility.
Beside Neisseria gonorrhea and Chlamydia trachomatis
playing as the two mostly frequently associated to upper
genital tract infections [4], the female genital tract is an
appropriate environment for the growth of other pathogenic
*Address correspondence to Minh Tam Le, M.D.,Ph.D, Associate Professor
at Department of Obstetrics and Gynecology, Hue University of Medicine and
Pharmacy, Hue University, Hue City, Vietnam; Tel/Fax: 0084.989228779; E-
mails: leminhtam@huemed-univ.edu.vn
DOI: 10.32895/UMP.MPR.4.2.3
© 2020 MedPharmRes
U. urealyticum and M. genitalium in Infertility
MedPharmRes, 2020, Vol. 4, No. 2 17
and non-pathogenic microorganisms. Mycoplasma is a
bacterium that can cause asymptomatic to minimally
symptomatic genital tract infections but can result in chronic
complications, including infertility. Previous published
studies have shown that Ureaplasma urealyticum and
Mycoplasma genitalium are responsible for lower genital tract
infections (vulvovaginitis) as well as upper genital tract
infections such as endometritis and pelvic inflammatory
disease [5-7]. M. genitalium was detected by swab from the
cervix in 19.6% of all infertile and in 4.4% of fertile women
[7]. Furthermore, the pregnancy rate after elimination of U.
urealyticum was significant improved [5]. Pelvic
inflammatory disease caused by these bacteria can induce
tubal disorders of varying degrees, including tubal occlusion
or hydrosalpinx.
birth. Exclusion criteria included being treated for genital
tract infection with local or systematic antibiotics within 4
weeks prior to inclusion, menorrhagia or declining
enrollment. The local ethics committee of Hue University of
Medicine and Pharmacy has approved this study, registration
number H2016/243. All participants were explained and
requested for written informed consent.
2.2. Survey method
All recruited women were interviewed following a
prepared protocol to obtain general characteristics including
age, occupation, geography, history of miscarriage, and
history of genital tract infection. A standardized pelvic
examination was then performed, and one vaginal swab was
taken for direct microscopic examination by wet mount. One
endocervical sample was also collected for detection of U.
urealyticum and M. genitalium by PCR.
U. urealyticum primarily colonizes in the human
urogenital tract and in the vaginal flora but it does not cause
disease under normal conditions, except when immunity is
impaired or the vaginal mucosa is damaged. However, the
impact of these infections to female infertility is still unclear.
Some authors reported that U. urealyticum and M. genitalium
may cause potential pathological effects on fertility in women
[5, 8], while other research has indicated no relation [9].
Whether U. urealyticum and M. genitalium are responsible
partly for infertility or whether this relationship is only
coincidental remains an unanswered question.
Hysterosalpingograms (HSGs) were indicated and
assessed by experienced doctors in all cases to investigate the
cavity of the uterus and fallopian tubes. First, a standard image
was obtained before the injection of contrast (Ultravist 300
(iopromide), Bayer, Leverkusen, Germany). Four images
were taken to assess the uterine cavity, tubal patency, and the
appearance of contrast medium in the pelvic cavity.
2.3. Laboratory test
Currently, it is not recommended for routine screening of
asymptomatic individuals for Mycoplasma hominis, U.
urealyticum, and U. parvum, because the asymptomatic
presence of these bacteria does not always develop disease.
However, cases with a high U. urealyticum load may be
benefit from treatment [10]. The widely indication of these
testing, diagnosis and accordingly treatment of these bacteria
may result in economic burden [10]. However, while
detection via PCR at a certain time cannot be causally linked
to prior damage, the presence of M. genitalium or U.
urealyticum may be associated with prior infection with a
traditional sexually transmitted urethritis-inducing agent, such
as Neisseria gonorrhoeae or Chlamydia trachomatis, which
may be related to secondary infertility. Furthermore, new
techniques of molecular methods have made the detection of
U. urealyticum and M. genitalium more feasible at high
sensitivity and specificity. So far, the recommendation of
screening U. urealyticum or M. genitalium to prevent the
complication of PID with severe tubal damage is still
controversial. The present study aimed to determine the
prevalence of U. urealyticum and M. genitalium infections in
cervical samples from secondarily infertile women and their
relationship to fallopian tube disorders.
Total DNA from the vaginal swab samples were
performed using iVApDNA Extraction Kit (Viet
A
Technology Corp., Ho Chi Minh, Vietnam)., following the
manufacturer’ instruction. The quality of total DNA were
checked using a NanoDrop 2000 spectrophotometer (Thermo
Fisher Scientific, Waltham, MA, USA). Conventional PCR
was performed using primers specifically targeting 540 bp of
the urease gene of U. urealyticum and 281 bp of the adhesin
gene of M. genitalium [11-14].
U. urealyticum
forward: 5′-AGAAGACGTTTAGCTAGAGG-3′
forward: 5′- AGTTGATGAAACCTTAACCCCTTGG-3′
M. genitalium
reverse: 5′-ACGACGTCCATAAGCAACT-3′
reverse: 5′- CCGTTGAGGGGTTTTCCATTTTTGC-3′
A total reaction volume reaction 25-μL reaction contained
5 μL DNA template, 0.4 μM each primer, and 12.5 μL 2×
GoTaq Green Master Mix (Promega, Madison, WI, USA).
PCR conditions for detection of U. urealyticum were as
follows: initial denaturation at 95°C for 4 min, 36 cycles of
95°C for 50 s, 55°C for 50 s, and 72°C for 60 s. Those for
detection of M. genitalium were as follows: initial
denaturation at 95°C for 5 min, followed by 36 cycles of 95°C
for 30 s, 65°C for 30 s, and 72°C for 30 s. PCRs were
performed on a Veriti™ 96-Well Thermal Cycler (Thermo
Fisher Scientific). PCR products were separated by 1%
agarose gel electrophoresis containing 1× GelRed™
(Biotium, Fremont, CA, USA) and digitalized with a Gel Doc
XR System (Bio-Rad, Hercules, CA, USA).
2. MATERIALS AND METHOD
2.1. Study population
Women with secondary infertility who underwent
treatment at the Center for Reproductive Endocrinology &
Infertility, Hue University Hospital, from July 2017 to July
2018 were enrolment for a cross-sectional descriptive study.
Inclusion criteria included women who were unable to get
clinical pregnant after 12 months of active sexual intercourse
or the inability to get a full-term pregnancy until a live
18 MedPharmRes, 2020, Vol. 4, No. 1
Le et al.
2.4. Data analysis
Infertility, Hue University Hospital, from July 2017 to July
2018, total of 95 cases were satisfied inclusion criteria with
mean age of 32.36 ± 4.72, 56.8% work in office, 63.2% lives
in non-urban area, 60% has educational levels from college
grade and 61.1% is secondary infertility more than three years.
There is 23.2% women with history of GTI and 63.2% with
history of miscarriage. Table 1 also shows that 73.7% of
patients had a normal vaginal microbiota. Among the 25 cases
with abnormal wet-mount, the most frequent infection type
was bacterial vaginosis (17.9%), with candidiasis accounting
for 7.4% of cases, aerobic vaginitis accounting for 2%, and
trichomoniasis accounting for 1.1%. Two cases of aerobic
vaginitis are co-infected with Candidiasis.
All analyses were performed using SPSS 20.0 (SPSS Inc.,
Chicago, IL, USA). An independent sample t-test was used
for normally distributed data or the Mann–Whitney U-test for
skewed data in comparison of continuous variables between
groups., the chi-square or Fisher’s exact test were used for
comparing categorical variables. Results are presented as odds
ratios (ORs) with 95% confidence intervals (CIs). p value
under 0.05 were considered significant statistically.
3. RESULTS
Table 1. Socio-demographic characteristics and gynecologic
examination of secondary infertile women
According to PCR of cervical samples from 95
secondarily infertile women, we detected 36 cases (37.9%)
positive for U. urealyticum and only two cases (2.1%) positive
for M. genitalia (Figure 1). There was no statistically
significant association between groups with positive PCR for
U. urealyticum as well as group with positive PCR for M.
genitalium and age, geography, occupation, education level,
history of genital tract infection, history of abdominal surgery,
or history of miscarriage, as shown in Table 3. Positive PCR
result for U. urealyticum was found to be associated with
bacterial vaginosis, with 2.86 times of higher rate of co-
infection (95% CI: 0.976–8.367, p = 0.05) while the two cases
positive for M. genitalium had normal vaginal microbiota.
Number
(n=95)
Percent
(%)
Characteristics
Age
< 35
67
28
70.5%
29.5%
≥ 35
Mean±SD
32.36 ± 4.72
Occupation
Manual work
Office work
Geography
Urban
41
54
43.2%
56.8%
Table 2. Hysterosalpingography results in secondary infertile
women
35
60
36.8%
63.2%
Non-urban
Hysterosalpingography results
Women with normal tubes
Occlusion 1 side
n
64
13
9
%
67.4
13.7
9.5
Educational levels
School grade
College / University grade
Infertility duration
< 3 years
38
57
40%
60%
Occlusion 2 sides
Hydrosalpinx 1 side
5
5.3
37
58
38.9%
61.1%
Hydrosalpinx 2 sides
Occlusion 1 side and Hydrosalpinx 1 side
Total
2
2.1
≥ 3 years
2
2.1
History of GTI
Yes
95
100
22
73
23.2%
76.8%
Among the 95 cases, normal HSG results were recorded in
64 cases, accounting for 67.4% of patients. Tube occlusion on
one or both sides was observed in 13.6% and 9.5% of cases,
respectively, and hydrosalpinx on one or both sides was
observed in 5.3% and 2.1% of cases, respectively (Table 2).
Analysis showed that a positive PCR result for U. urealyticum
was correlated with an abnormal HSG in secondarily infertile
women, increasing the rate of an abnormal HSG result by
2.88-fold (95% CI: 1.18–6.99, p = 0.018) (Table 4).
No
History of miscarriage
Yes
60
35
63.2%
36.8%
No
Wet-mount results
Normal microbiota
Abnormal
70
25
17
7
73.7%
26.3%
17.9%
7.4%
Bacterial vaginosis
Candidiasis
Trichomoniasis
4. DISCUSSION
U. urealyticum and M. genitalium have been reported to
be associated with female infertility in some studies [15, 16].
M. genitalium has been detected in 5.7% (10/176) of the total
population and in 5.6% (9/161) of those with symptoms,
corresponding to 5.7% (5/87) of symptomatic men and 5.4%
(4/74) of symptomatic women [17]. Ureaplasma was also
diagnosed in 25.8% of patients with genital tract infections
and 20.8% of infertile women [18]. According to Peerayeh et
1
1.1%
Aerobic vaginitis*
GTI: genital tract infection
*Two cases of aerobic vaginitis were co-infected with
Candidiasis
By screening all women with secondary infertility who
were treated at the Center for Reproductive Endocrinology &
2
2.1%
U. urealyticum and M. genitalium in Infertility
MedPharmRes, 2020, Vol. 4, No. 2 19
al., 30.7% of infertile women were positive for Ureaplasma
or Mycoplasma, among which 51.7% were positive for
Ureaplasma, 26.7% for Mycoplasma, and 21.5% for both
[19]. Similarly, Grzesko et al. found a prevalence of M.
genitalium infection of 19.6% in infertile women [5]. A
population‐based study of M. genitalium in Vietnam reported
a significantly low prevalence in reproductive age women in
rural areas (0.8%; 95% confidence interval, 0.25–1.35%) [20].
Table 3. Prevalence and the risk factors of positive PCR for U. urealyticum and M. genitalium in secondary infertile women
Positive PCR for M.
Positive PCR for U. urealyticum
genitalium
p-value
p-value
n=36
n=2
Characteristics
n / Total
(%)
n / Total (%)
OR (95% CI)*
OR (95% CI)*
Age
< 35
≥ 35
Occupation
Manual work
Office work
Geography
24 (35.8)
0.74
2 (3.0%)
0
0.415
1.17
-
1
1
12 (42.9%)
[0.30-1.83]
13 (31.7%
23 (42.6%)
1.60
1 (2.4%)
1 (1.9%)
0.76
[0.68-3.74]
[0.05-12.44]
Urban
15 (42.9%)
21 (35.0%)
1.39
0
0.58
-
0.53
1
Non-urban
[0.59-3.27]
2 (3.3%)
Educational levels
School grade
College / University grade
Infertility duration
< 3 years
12 (31.6%)
24 (42.1%)
0.64
1 (2.6%)
1 (1.8%)
1.51 [0.09-
24.96]
0.30
[0.27-1.50]
15 (40.5%)
21 (36.2%)
1.201
1 (2.7%)
1 (1.7%)
1.583
0.18
1
≥ 3 years
[0.52-2.80]
[0.10-26.11]
History of GTI
Yes
10 (45.5%)
26 (35.6%)
1.51
1 (4.5%)
1 (1.4%)
3.43
0.695
0.104
0.41
0.53
No
[0.57-3.96]
[0.21-57.18]
History of miscarriage
Yes
22 (36.7%)
14 (40.0%)
0.868
2 (3.3%)
0
No
[0.37-2.04]
Wet-mount results
Normal microbiota
Abnormal
23 (32.9%)
13 (52%)
2 (100%)
0
2.857
Bacterial vaginosis
Candidiasis
10 (58.8%)
2 (28.6%)
0.05
[0.976-8.367]
0.653
0.706
[0.117-3.460]
Trichomoniasis
1 (100%)
2 (100%)
0.379
0.141
Aerobic vaginitis **
U. urealyticum: Ureaplasma urealyticum; M. genitalium: Mycoplasma genitalium; GTI: genital tract infection
* non-adjusted odds ratio; ** these 2 cases of aerobic vaginitis were detected in coinfection with Candidiasis.
20 MedPharmRes, 2020, Vol. 4, No. 1
Le et al.
Figure 1. PCR amplification analysis for the detection of (A) U. urealyticum and (B) M. genitalium. PCR products
were separated on a 1.0% agarose gel. Lane SM is a DNA size marker (GeneRuler 100 bp DNA Ladder - Thermo
Fisher Scientific); in lane PC, M. genitalium (ATCC® 33530D™) and U. urealyticum (ATCC® 29559™) were
used as positive controls; lane NC is a non-template control; lanes 3–8 are genomic DNAs from vaginal swab
samples.
Table 4. Correlation between PCR-positive cases for U. Urealyticum and M. genitalium and hysterosalpingography results
Abnormal HSG
Normal HSG
Genital tract infection
p*-value
OR (95% CI)
n
%
n
%
U. urealyticum
Positive
2.88
17
14
47.2
23.7
19
45
52.8
76.5
0.018
[1.18- 6.99]
Negative
M. genitalium
Positive
0
2
100
66.7
67.4
1
Negative
31
31
33.3
32.6
62
64
Total
HSG: hysterosalpingography
Our study revealed that the prevalences of U. urealyticum
and M. genitalium in cervical samples of secondarily infertile
patients were 37.9% and 2.1%, respectively. Compared to
community studies of infertile individuals, this shows a
similar or higher prevalence of U. urealyticum infection.
Atefeh et al. reported similar results, with prevalence of U.
urealyticum and M. genitalium of 37.5% and 2.9% in 104
infertile women [21]. Sleha et al. found that the prevalence of
U. urealyticum infection in 111 infertile women was 39.6%
[22], and Melih et al. found that a U. urealyticum infection
rate of 42% among women with unexplained infertility [6].
Seifoleslami et al. found that the prevalence of U. urealyticum
in infertile women was significantly higher than that in
women without infertility [3], and this pattern was also
observed in a study by Al-Kayat with 150 infertile and 150
non-infertile women showing prevalences of 22% and 4.7%,
respectively [5]. Grześko et al. reported that subjects with
vaginal discharge showed a significantly higher incidence of
U. urealyticum than the asymptomatic group [7]. A study by
Benu et al. in adult women with abnormal discharge revealed
that the prevalence of U. urealyticum infection as detected by
PCR was 45% [18].
acute infection. According to Horner et al., routine testing of
asymptomatic persons for U. urealyticum is not
recommended. This is because detection by PCR shows the
presence of a microorganism but does not confirm an infection
and therefore cannot indicate whether the microorganism has
caused tubal damage prior to testing for infertility [10].
In our study, among women with a positive PCR result for
U. urealyticum, the prevalence of an abnormal HSG result was
47.2%, while in women without a positive U. urealyticum
result, the prevalence of an abnormal HSG was only 23.7%.
The two patients with M. genitalium infection had normal
HSGs. There was a statistically significant relation between
U. urealyticum infection and an abnormal HSG. An early
study by Henry-Suchet et al. performed laparoscopic
examination on 99 women in three groups: (1) 17 with acute
pelvic inflammatory disease, (2) 46 with tubal infertility
without pelvic inflammatory disease, and (3) a control group
of 36 women with infertility due to other causes [23]. The
results showed that U. urealyticum was present in 17% of the
specimens collected from the fallopian tubes or peritoneum of
the experimental groups and only 5% of those from the control
group. Among infertile women with occluded fallopian tubes,
the prevalence of U. urealyticum infection was five times
higher than that of the infertile women with normal tubes, but
this difference was not statistically significant [24]. A study in
Spain found that in infertile women, Ureaplasma infection
rates were 21.7%, and among 10 cases with Ureaplasma
In fact, as demonstrated by the abovementioned studies,
research has shown a high prevalence of U. urealyticum in
cervical swaps. However, there is less evidence determining
the relationship between the presence of a microorganism as
detected by PCR of a sample taken at a given time and an
U. urealyticum and M. genitalium in Infertility
MedPharmRes, 2020, Vol. 4, No. 2 21
present, an abnormal HSG was recorded in seven cases [25].
However, this statistically difference was not significant due
to the small sample size.
This research did not receive any specific grant from any
funding agency in the public, commercial or not-for-profit
sectors.
Studies on M. genitalium have also shown high infection
rates in infertile patients. A study by Nonika and colleagues
in women with infertility in India showed that the prevalence
of M. genitalium infection was 16% among specimens from
the urine, cervix, or endometrium, while no infections were
detected in non-infertile women [26]. Rates of occlusion and
endometrial hyperplasia were 33% and 26.66%, respectively,
among those positive for M. genitalium [26]. Svenstrup et al.
studied 194 women with tubal disease and showed that 17%
of patients had anti-M. genitalium antibodies, compared with
only 4% of women with normal uterine tubes; additionally,
14% of patients with a history of pelvic inflammatory disease
were positive for M. genitalium, compared with 6% of patients
with no history of PID [27]. However, in our study, only 2/95
women with secondary infertility were positive for M.
genitalium, so it was not possible to assess associations with
other factors.
CONFLICTS OF INTEREST
The authors report no conflicts of interest. The authors
alone are responsible for the content and writing of this article.
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In the case of women with secondary infertility, genital
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urealyticum infection was high and appeared to be associated
with tubal damage.
AUTHOR CONTRIBUTIONS
M.T.L, Q.D.L, V.Q.H.N participated in the study design,
execution, analysis, manuscript drafting and critical
discussion. V.Q.T.N, H.B.N, participated in the study
execution, manuscript drafting and critical discussion. All
authors have read and approved the final manuscript.
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