Prevalence and risk factors of Ureplasma urealyticum and Mycoplasma genitalium among women with secondary infertility in Vietnam – A crosssectional study

 16 MedPharmRes, 2020, 4 
*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 
MedPharmRes 
journal of University of Medicine and Pharmacy at Ho Chi Minh City 
homepage:  and  
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 
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 
uterine or peritoneal diseases are most common, whereas tubal 
disorder is the second common causes of secondary infertility 
in women [3]. 
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 
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. 
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 reporte ... plasma, 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 
Characteristics 
Positive PCR for U. urealyticum 
n=36 
p-value 
Positive PCR for M. 
genitalium 
n=2 
p-value 
n / Total (%) OR (95% CI)* 
n / Total 
(%) 
OR (95% CI)* 
Age 
< 35 24 (35.8) 0.74 
[0.30-1.83] 
0.415 
2 (3.0%) 
- 1 
≥ 35 12 (42.9%) 0 
Occupation 
Manual work 13 (31.7% 1.60 
[0.68-3.74] 
1.17 
1 (2.4%) 0.76 
[0.05-12.44] 
1 
Office work 23 (42.6%) 1 (1.9%) 
Geography 
Urban 15 (42.9%) 1.39 
[0.59-3.27] 
0.58 
0 
- 0.53 
Non-urban 21 (35.0%) 2 (3.3%) 
Educational levels 
School grade 12 (31.6%) 0.64 
[0.27-1.50] 
0.30 
1 (2.6%) 1.51 [0.09-
24.96] 
1 
College / University grade 24 (42.1%) 1 (1.8%) 
Infertility duration 
< 3 years 15 (40.5%) 1.201 
[0.52-2.80] 
0.18 
1 (2.7%) 1.583 
[0.10-26.11] 
1 
≥ 3 years 21 (36.2%) 1 (1.7%) 
History of GTI 
Yes 10 (45.5%) 1.51 
[0.57-3.96] 
0.695 
1 (4.5%) 3.43 
[0.21-57.18] 
0.41 
No 26 (35.6%) 1 (1.4%) 
History of miscarriage 
Yes 22 (36.7%) 0.868 
[0.37-2.04] 
0.104 
2 (3.3%) 
 0.53 
No 14 (40.0%) 0 
Wet-mount results 
Normal microbiota 23 (32.9%) 2 (100%) 
Abnormal 13 (52%) 0 
 Bacterial vaginosis 10 (58.8%) 
2.857 
[0.976-8.367] 
0.05 
 Candidiasis 2 (28.6%) 
0.653 
[0.117-3.460] 
0.706 
 Trichomoniasis 1 (100%) 0.379 
 Aerobic vaginitis ** 2 (100%) 0.141 
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. 
Table 4. Correlation between PCR-positive cases for U. Urealyticum and M. genitalium and hysterosalpingography results 
Genital tract infection 
Abnormal HSG Normal HSG 
p*-value OR (95% CI) 
n % n % 
U. urealyticum 
0.018 
2.88 
[1.18- 6.99] 
Positive 17 47.2 19 52.8 
Negative 14 23.7 45 76.5 
M. genitalium 
1 Positive 0 2 100 
Negative 31 33.3 62 66.7 
Total 31 32.6 64 67.4 
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]. 
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 
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 
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. 
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. 
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. 
Limitation of the current study is that the detection of M. 
genitalium and U. urealyticum by PCR will show the 
presence of a microorganism but not infection and not 
ensure that the microorganism has caused tubal damage 
prior to testing for infertility. Therefore, it would be more 
relevant to test for antibodies to the microorganisms of 
interest, as the presence of antibodies would indicate a 
previous infection. In addition, abnormal HSG findings could 
also be caused by other co-infections not tested for, such as C. 
trachomatis and N. gonorrhoeae. 
In conclusion, previous research has revealed important 
complications involving U. urealyticum and M. genitalium 
infection, but prevalence appears to vary in different 
populations. Our data showed that in secondarily infertile 
women, the presence of M. genitalium was rare whereas the 
proportion positive for U. urealyticum according to PCR was 
high. The presence of this bacterium may be associated with 
tubal damage. It is therefore necessary to routinely screen for 
U. urealyticum for better diagnosis and management of 
secondary infertility. 
5. 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. 
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. 
ACKNOWLEDGEMENTS 
This research did not receive any specific grant from any 
funding agency in the public, commercial or not-for-profit 
sectors. 
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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