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Ureaplasma urealyticum and Ureaplasma parvum in women of reproductive age

Blaženka Hunjak,1 Ivan Sabol,2 Gordana Vojnović,3 Ivan Fistonić,4 Andrea Babić Erceg,3
Zdenka Peršić,1 Magdalena Grce2

1
Department of Microbiology and Bacteriology, Croatian National Institute of Public Health,
Rockefellerova 2, 10000Zagreb, Croatia
2
Department of Molecular Medicine, Rudjer Boskovic Institute, Bijenicka 54, 10000 Zagreb,
Croatia
3
Department of Molecular Diagnostics, Croatian National Institute of Public Health,
Rockefellerova 2, 10000Zagreb, Croatia
4
Private Gynaecological Clinic, Preradoviceva 10, 10000 Zagreb, Croatia

Corresponding author:

Magdalena Grce, PhD, Department of Molecular Medicine, Rudjer Boskovic Institute, Bijenicka
54, 10000 Zagreb, Croatia; grce@irb.hr

1
Abstract

Objectives. To determine the incidence of Ureaplasma urealyticum (UU) and Ureaplasma

parvum (UP) in symptomatic and asymptomatic women of reproductive age and to estimate
antibiotic susceptibility of ureaplasma isolates.

Material and methods. This study included 424 ureaplasma positive women of 1370 tested
women who visited gynecological practices during 2010. Cervicovaginal or urethral swab
specimens from each patient were obtained for cultivation and molecular typing by RT-PCR.

Results. Ureaplasma spp. was identified by cultivation in 424 (34.4%) cases, of which 79.0%
were from women with symptoms and 21.0% from women without symptoms. Among
ureaplasma positive women, 121 (28.5%) were pregnant. Genotyping was successful in 244
strains, and the majority of samples were identified as UP (92.6%). Among genotyped isolates,
there were 79.5% from symptomatic and 20.5% from asymptomatic women; 29.9% from
pregnant and 70.1% from non-pregnant women. There was no difference in the incidence of
ureaplasma type regarding symptoms. Antibiotic susceptibility of 424 ureaplasma isolates
identified by cultivation showed that all strains were susceptible to doxycycline, josamycin,
erythromycin, tetracycline, clarithromycin and pristinamicin, but there was lower susceptibility
to quinolone antibiotics, i.e. 42.9% and 24.5% isolates were susceptible to ofloxacin and
ciprofloxacin, respectively.

Conclusion. This study shows that UP was the most frequent isolated ureaplasma species
(92.6%). Regarding antibiotic susceptibility, quinolones are not the best choice for treatment of
ureaplasma infections, while macrolides and tetracyclines are still effective.

Introduction

Urogenital ureaplasma in women of childbearing age are associated with urethritis, pelvic
inflammatory disease, pregnancy complications, premature birth and infertility but are also very
frequent in healthy women. Mycoplasmas are the smallest known free living microorganisms of
200 to 300 nm in size. Taxonomically, mycoplasmas belong to the class of Mollicutes together
with ureaplasma, also called T (tiny) mycoplasmas because they produce a very small colony
size of only 50-60 micrometer in diameter [1]. In humans, urogenital ureaplasma infection is

2
caused by two species, Ureaplasma urealyticum (UU) and Ureaplasma parvum (UP), with a
total of 14 serotypes. UU has characteristics of biovar T960T (or biovar 2 or A), and includes 10
large genomic serovars (0.88-1.2 Mbps): 2, 4, 5, 7, 8, 9, 10, 11, 12 and 13, while UP has
characteristics of parvo biovar (or biovar 1 or B) and includes four serovars: 1, 3, 6 and 14 [2,3].

In the urogenital system UU and UP are considered pathogenic isolates. In women, the
urogenital tract infection can be asymptomatic or with mild to severe symptoms, while in men
ureaplasma commonly causes urethritis. If the infection spreads to the uterus or fallopian tubes in
women or in the small bowel it may lead to pelvic inflammatory disease. The role of ureaplasma
in pregnant women is of particular importance as the infection may lead to complications in
pregnancy resulting in premature labour, miscarriage or stillborn child [2,4–9]. Undiagnosed and
untreated infection can also lead to infertility. When determining the clinical significance of
ureaplasma infection, the differentiation of colonization and infection is necessary because of the
high prevalence of ureaplasmas in the healthy population (ureaplasma 70-80%, mycoplasmas 30-
40%) [10]. The presence of more than 104 CFU in a sample is an additional criterion to
distinguish colonization from infection.

Although considered “gold standard”, culture methods could not differentiate species, UU from
UP. Therefore, it is important to introduce molecular methods such as real-time polymerase
chain reaction (RT-PCR), which enables distinguishing ureaplasma species [11,12]. The
objectives of this study were to determine the incidence of UU and UP in symptomatic and
asymptomatic women of reproductive age and to estimate antibiotic susceptibility of ureaplasma
isolates.

Material and methods

Study population

The study was carried out at Gynecological Practices of Primary Health Centers in Zagreb,
Croatia which are collaborating institutions of the Croatian National Institute of Public Health.
Of 1370 women who visited gynaecological practices during 2010, 471 women were positive for
ureaplasma isolates. Only 424 isolates were included in the analysis as for 47 isolates complete

3
medical records were not available. Of the total number of ureaplasma positive women 121
(28.5%) were pregnant. Women were divided in two groups, 89 (21.0%) asymptomatic women
who came to the gynaecological examination because of a routine check-up, or disease
conditions that were not related to urogenital system, and 335 (79.0%) symptomatic women who
had at least one of the following symptoms: non-specific pain and tension in the lower abdomen,
increased vaginal discharge, dispareunia, burning and frequent urination. The age of
symptomatic women ranged from 16 to 64 years (mean 31.6; median 30), while the age of
asymptomatic women ranged from 20 to 68 years (mean 30.7; median 30).

Specimen collection

Cervicovaginal or urethral swab specimens were collected for microbiological and molecular
analysis. All specimens were obtained before antibiotic treatment. Ureaplasma cultivation was
performed at the Department of Bacteriology, while the RT-PCR analysis was performed at the
Department of Molecular Diagnostics of the Croatian National Institute of Public Health.

Bacterial detection and antimicrobial susceptibility

Ureaplasma identification was done by cultivation on agar and liquid medium, as well as with a
commercial Mycoplasma IST 2 (BioMerieux, Marcy l'Etoile, France). The test is based on the
principle of metabolic inhibition of sensitive strains. This test allows the cultivation,
identification, determination of the indicative number of bacteria and determine the susceptibility
of the isolates to antibiotics [13,14].

Co-infection with other microorganisms including Gardnerella vaginalis (GV) , beta-haemolytic

Group B Streptococcus (GBS), Candida albicans (CA) was identified according to routine
laboratory methods, including API-tests (BioMérieux SA Marcy l'Etoile, France). Chlamydia
trachomatis (CT) identification was done with COBAS AMPLICOR CT/NG Test (Roche, Basel,
Switzerland) and according to Airell et al. [15].

Real-time PCR

Two hundred eighty six samples for which the Mycoplasma IST 2 test result was ≥ 104 CFU
were used in subsequent identification with RT-PCR. Ureaplasma isolates were stored at -20° C
until DNA isolation procedure with the commercial assays (QUIamp DNA Mini Kit; QUIAGEN

4
GmbH, Hilden) according to the manufacturer's instructions. Differentiating strains of UU of UP
was performed as described by Mallard et al. [12].

Statistical analysis

Data and statistical analysis was performed in the Division of Molecular Medicine, Rudjer
Boskovic Institute using GraphPad Prism (version 4.00) (GraphPad Software, San Diego,
California, USA). Methods of descriptive statistics, Chi square (χ2)-test and Fishers exact test
were used. The P-values of <0.05 were considered statistically significant.

Results

Of the 424 samples, 286 (67.4%) were analyzed by RT-PCR. In 42/286 (14.6%) samples the
PCR failed to identify ureaplasma species, due to technical difficulties, while 244 samples were
successfully genotyped (Table 1). There were 18 (7.4%) samples identified as UU and 226
(92.6%) as UP. Of 18 UU cases, 15 (83.3%) were isolated in symptomatic and three (16.7%) in
asymptomatic women, while of 226 UP cases 179 (79.2%) and 47 (20.8%) were isolated in
symptomatic and asymptomatic women, respectively. There were no statistically significant
difference between the incidence of UU and UP among symptomatic and asymptomatic women
(P = 0.676).

In the group of pregnant women, UU and UP were isolated in 4/18 (22.2%) and 69/226 (30.5%)
women, respectively. In the group of women who were not pregnant, UU was isolated in 14/18
(77.8%), while UP was isolated in 157/226 (69.5%) women (Table 1). There were no statistically
significant difference between the incidence of UU and UP among pregnant and non-pregnant
women (P = 0.459).

Table 2 presents subgroups of samples including both pregnancy and symptoms data. Statistical
significance (Chi – square test P = 0.022) was observed in UU and UP isolation in the non-
pregnant subset where UU appeared more often in asymptomatic infections than UP. However,
this difference is probably due to very limited number of asymptomatic infections in this subset
(n=6). Using Fishers exact test, which is more suitable for small sample sizes, statistical
difference was not found (P =0.077) . Subset of samples including only pregnant women did not
indicate statistically significant difference of ureaplasma species isolation in women with or
without symptoms (P = 0.138).

5
In a cohort of symptomatic women who were not pregnant, UP was found in 153 of 157 (97.5%)
cases, while UU in 12 of 14 (85.7%) cases. In a cohort of asymptomatic women who were not
pregnant, UP was found in 4 of 157 (2.5%) cases, while UU in 2 of 14 (14.3%) cases.

In a cohort of symptomatic pregnant women UP was found in 26 of 69 (37.7%) cases, while UU

in 3 of 4 (75.0%) cases. In asymptomatic pregnant women UP was found in 43 of 69 (62.3%)
cases, while UU in 1 of 4 (25.0%) cases.

In genotyped ureaplasma isolates, simultaneously associated microorganisms (Table 3) were GV

(20.1%), CA (11.1%), GBS(4.1%), and CT (3.7%). However, there was no significant
differences between UU and UP species in co-isolated microorganisms.

Antibiotic susceptibility of 424 ureaplasma isolates identified by cultivation (Table 4) showed

that all strains were sensitive to doxycycline, josamycin, erythromycin, tetracycline,
clarithromycin, and pristinamicin. Only one ureaplasma isolate showed moderate susceptibility
to azithromycin. In addition, there was some resistance to quinolone antibiotics.

The antibiotic susceptibility of 244 ureaplasma genotyped by RT-PCR showed that all strains of
UU and UP were sensitive to doxycycline, josamycin, erythromycin, tetracycline, clarithromycin
and pristinamicin even though some isolates were resistant to quinolone antibiotics (Table 4).
Lower sensitivity was observed to ofloxacin (42.9%) and ciprofloxacin (24.5%). One UU isolate
(0.3%) showed moderate susceptibility to azithromycin. Regarding genotyped ureaplasma
isolates, there were 72.2% UU isolates resistant to ciprofloxacin,

Discussion

In recent years urogenital ureaplasmas are highly frequent isolated in women of childebearing
age. Prior to this study the prevalence of different ureaplasma species was not well studied for
the Croatian population. This study showed 34.3% positive samples of urogenital tract in the
female population. Zdorowska-Stefanov et al. [16] found slightly lower ureaplasma prevalence
(29.8% of 541 women tested), while Kechagia et al. [17] found slightly higher prevalence
(37.0% of 369 women tested). Molecular based studies have shown that most of ureaplasma
isolates thus far considered UU were actually UP [18–20]. According to Kacerovský et al. [21],
the prevalence of UP in a cohort of healthy women who were not pregnant was 57%, which is a

6
much higher prevalence than those of other genital mycoplasmas, viruses, Chlamydia or GBS
infections.

In this study, most ureaplasma isolates were identified as UP (92.6%) as expected [18,21,22].
We found no significant differences between UP or UU positive individuals according to
symptoms or pregnancy. There are evidence of adverse impact of ureaplasma infection on the
course and outcome of pregnancy [2,4], and that ureaplasma infection in infants is associated
with low birth weight and perinatal mortality [23]. Govender et al. [24] established ureaplasma
high prevalence among women aged ≥ 26 years. However, association between colonization of
Mycoplasma hominis, UU or UP and premature births was not confirmed. Results of this study
showed that the UU and UP were almost equally often isolated in women who were pregnant or
not (22.2%; vs. 30.5%).

Women of reproductive age often suffer from urogenital infections. In this study incidence of
other concomitant bacteria and fungi with ureaplasma was investigated. Common isolated
microorganisms with ureaplasma were GV (20.1%), CA (11.1%), GBS (4.1%), and CT (3.7%).
The results are consistent with a study of Vogel et al. [25] who found GV the most common
isolate with ureaplasma. In our study CA has been isolated in women with UP (11.9%), but no in
patients with UU. Since CA causes unpleasant clinical symptoms, we believe that co-infection
with CA and UP should be investigated in a large number of samples. Despite the significant role
of CT infection in genitourinary tract, in our study it was found in only 3.7% of women.

In this study, the antibiotic sensitivity of ureaplasma isolates identified by cultivation showed
that all strains were sensitive to doxycycline, josamycin, erythromycin, tetracycline,
clarithromycin and pristinamicin, but some resistance to quinolones was observed. Limited
sensitivity was observed with ofloxacin (42.9%) and ciprofloxacin (24.5%). One UU (0.3%)
isolate showed moderate resistance to azithromycin. In addition, regarding the genotyped
ureaplasma isolates, where 72.2% of UU isolates were resistant to ciprofloxacin, it can be
concluded that quinolones are not the best choice for treatment of ureaplasma isolates. These
findings are consistent with research of Baryaktar et al. [23] who estimated higher resistance to
quinolones of UU, i.e. 86.2% to ofloxacin and 92.6% to ciprofloxacin. The study of Mares et al.
[26] showing resistance to ofloxacin was 16.1% and 53.8% to ciprofloxacin also support the

7
findings in this study. However, it can be concluded that macrolides and tetracyclines are still
high effective in ureaplasma infection treating.

Conclusion

In this study, both species of ureaplasma, UP and UU, appeared in women regardless of
symptoms or pregnancy with UP being the predominant species in the Croatian population. Due
to small number of UU samples it is so far impossible to determine differences in pathogenicity
between UP and UU and further large scale studies should be done to elucidate potential
differences.

Acknowledgement

Authors thank Dr Irena Tabain for technical assistance, Dr Štefica Findri-Guštek and Dr Jean
Chedid for sample collection. This research has been partially supported by the Ministry of
Science, Education and Sports (Grant number: 098-0982464-2510).

Conflict of interest

The authors have declared that no competing interests exist.

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24. Govender S, Theron GB, Odendaal HJ, Chalkley LJ (2009) Prevalence of genital
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Abstract

Objectives. To determine the incidence of Ureaplasma urealyticum (UU) and Ureaplasma

parvum (UP) in symptomatic and asymptomatic women of reproductive age and to estimate
antibiotic susceptibility of ureaplasma isolates.

Material and methods. This study included 424 ureaplasma positive women of 1370 tested
women who visited gynecological practices during 2010. Cervicovaginal or urethral swab
specimens from each patient were obtained for cultivation and molecular typing by RT-PCR.

Results. Ureaplasma spp. was identified by cultivation in 424 (34.4%) cases, of which 79.0%
were from women with symptoms and 21.0% from women without symptoms. Among
ureaplasma positive women, 121 (28.5%) were pregnant. Genotyping was successful in 244
strains, and the majority of samples were identified as UP (92.6%). Among genotyped isolates,
there were 79.5% from symptomatic and 20.5% from asymptomatic women; 29.9% from
pregnant and 70.1% from non-pregnant women. There was no difference in the incidence of
ureaplasma type regarding symptoms. Antibiotic susceptibility of 424 ureaplasma isolates
identified by cultivation showed that all strains were susceptible to doxycycline, josamycin,
erythromycin, tetracycline, clarithromycin and pristinamicin, but there was lower susceptibility
to quinolone antibiotics, i.e. 42.9% and 24.5% isolates were susceptible to ofloxacin and
ciprofloxacin, respectively.

Conclusion. This study shows that UP was the most frequent isolated ureaplasma species
(92.6%). Regarding antibiotic susceptibility, quinolones are not the best choice for treatment of
ureaplasma infections, while macrolides and tetracyclines are still effective.

12
Table 1. Ureaplasma genotypes in women according to symptoms and pregnancy status

Ureaplasma isolates

U. urealyticum U. parvum Total P value

(n = 18) (n=226) (n=244)

Symptomatic infection

Yes 15 (83.3%) 179 (79.2%) 194 (79.5%)

0.676
No 3 (16.7%) 47 (20.8%) 50 (20.5%)

Pregnancy

Yes 4 (22.2%) 69 (30.5%) 73 (29.9%)

0.459
No 14 (77.8%) 157 (69.5%) 171 (70.1%)

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Table 2. Ureaplasma genotypes in pregnant and non-pregnant women

Ureaplasma isolates
P value
U. urealyticum U. parvum Total

Non-pregnant women

Symptomatic
12 (85.7%) 153 (97.5%) 165(96.5%)
infection
0.077*
Asymptomatic
2 (14.3%) 4 (2.5%) 6 (3.5%)
infection

Subtotal 14 157 171

Pregnant women

Symptomatic
3 (75.0%) 26 (37.7%) 29 (39.7%)
infection
0.138
Asymptomatic
1 (25.0%) 43 (62.3%) 44 (60.3%)
infection

Subtotal 4 69 73
* Fishers exact test

14
Table 3. Microorganisms associated with U. parvum and U. urealyticum

Ureaplasma isolates

Microorganisms U. urealyticum U. parvum Total

P value
(n = 18) (n=226) (n=244)

G. vaginalis 3 (16.7) 46 (20.4) 49 (20.1) 0.707

C. albicans 0 27 (11.9) 27 (11.1) 0.119

GBS 1 (5.6) 9 (4.0) 10 (4.1) 0.746

C. trachomatis 1 (5.6) 8 (3.5) 9 (3.7) 0.662

Other
12 (66.6) 142 (62.8) 154 (63.1) 0.746
microorganisms*

*microorganisms isolated in small numbers and urogenital physiological flora

15
Table 4. Antimicrobial susceptibility of the total isolated ureaplasma and of specific genotype

Ureaplasma parvum
Ureaplasma isolates (N=424) Ureplasma urealyticum (N=18)
Antimicrobial (N=226)
agent
S I R S I R S I R

Doxycycline 424 (100%) 0 0 18 (100%) 0 0 226 (100%) 0 0

Josamycin 424 (100%) 0 0 18 (100%) 0 0 226 (100%) 0 0

122
Ofloxacin 182 (42.9%) 220 (51.9%) 22 (5.2%) 5 (27.8%) 12 (66.7%) 1 (5.5%) 94 (41.6%) (54.0 10 (4.4%)
%)

Erythromycin 424 (100%) 0 0 18 (100%) 0 0 226 (100%) 0 0

Tetracycline 424 (100%) 0 0 18 (100%) 0 0 226 (100%) 0 0

107
Ciprofloxacyn 104 (24.5%) 170 (40.1%) 150 (35.4%) 2 (11.1%) 3 (16.7%) 13 (72.2%) 40 (17.7%) (47.3 79 (35.0%)
%)

Azithromycin 423 (99.7%) 1 (0.3%) 0 17 (99.9%) 1 (0.1%) 0 226 (100%) 0 0

Clarithromycin 424 (100%) 0 0 18 (100%) 0 0 226 (100%) 0 0

Pristinamicin 424 (100%) 0 0 18 (100%) 0 0 226 (100%) 0 0

S, susceptible, I, intermediate, R resistant

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17