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Effects of Chlamydia trachomatis Infection on Fertility; A Case-Control Study

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Original Article

Effects of Chlamydia trachomatis Infection on Fertility; A Case-Control

Study
Batool Hossein Rashidi 1, Leili Chamani-Tabriz 2, 3*, Fadieh Haghollahi 1, Mahmood Jeddi-Tehrani 4, Mohammad
Mehdi Naghizadeh 5, Mamak Shariat 6, Mohammad Mehdi Akhondi 2, Rezvan Bagheri 2, Soheila Asgari 2,7,
Kevan Wylie 8

1- Vali-e-Asr Reproductive Health Research Center, Tehran University of Medical Sciences, Tehran, Iran
2- Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran
3- Infectious Diseases and Tropical Medicine Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
4- Monoclonal Antibody Research Center, Avicenna Research Institute, ACECR, Tehran, Iran
5- Department of Biostatistics and Epidemiology, Fassa University of Medical Sciences, Fassa, Iran
6- Maternal-Fetal-Neonatal Health Research Center, Tehran University of Medical Sciences, Tehran, Iran
7- International Campus, Tehran University of Medical Sciences, Kish, Iran
8- Consultant in sexual Medicine, Sheffield, UK

Abstract
Background: Nowadays, Chlamydia trachomatis is known as a causative agent of
infertility. Because of, asymptomatic nature of infection, many may suffer from its
lasting complications such as infertility. This study was performed in Tehran during
April 2007 to April 2008 to compare the prevalence of Chlamydia trachomatis infec-
tion in fertile and infertile women using ELISA and PCR methods.
Methods: Overall, 234 infertile and 223 pregnant women, as the fertile group, par-
ticipated in this hospital-based case-control study. After completing an informed
consent form and the questionnaire, first catch urine and blood sample were obtained
for PCR and ELISA (IgG, IgM) tests, respectively. Logistic regression analysis was
used to control possible confounding factors, and determine adjusted odds ratio of
infertility due to the infection.
* Corresponding Author: Results: PCR results revealed that 29 (12.4%) of the infertile and 19 (8.5%) of the
Leili Chamani-Tabriz,
Reproductive Biotechnol-
fertile women were positive for C. trachomatis infection (p=0.440). IgG was positive
ogy Research Center, in 21 (9.0%) of the infertile and 11 (5.0%) in the fertile group (p=0.093). IgM assays
Avicenna Research Insti- identified that 2 (0.9%) of the infertile and 4 (1.8%) of the fertile women were posi-
tute, ACECR, Tehran, Iran tive for the micro-organism (p=0.375).
E-mail:
Conclusion: We found no significant differences among fertile and infertile women
lchamani@[Link]
for Chlamydia trachomatis infection. Nevertheless, molecular techniques which are
Received: Aug. 18, 2012 more sensitive, more specific and non-invasive can be used to detect C. trachomatis
Accepted: Nov. 28, 2012 infection.

Keywords: Case control study, Chlamydia trachomatis, Enzyme-linked immunosorbent as-

say, Infertility, Polymerase chain reaction.
To cite this article: Hossein Rashidi B, Chamani-Tabriz L, Haghollahi F, Jeddi-Tehrani M,
Naghizadeh MM, Shariat M, et al. Effects of Chlamydia trachomatis Infection on Fertility; A
Case-Control Study. J Reprod Infertil. 2013;14(2):67-72.

Introduction
hlamydia trachomatis is the most common unreported in the United States during 2004 (2).
sexually transmitted bacterial infection (1). Vaginal discharge, dysuria, postcoital bleeding,
More than 900.000 infections with C. tra- intermenstrual bleeding and abdominal pain are
chomatis were reported and twice as many were some of the symptoms that are associated with

J Reprod Infertil. 2013;14(2):67-72

 Hossein Rashidi B, et al. JRI
genital infection with C. trachomatis in women Methods
(3). This type of bacterial infection may be asymp- Setting: This case-control study was performed at
tomatic and delay in its diagnosis may cause the infertility clinic, prenatal clinic and delivery
harmful effects but early detection and appropriate room of Vali-e-Asr Hospital, one of the central
treatment can minimize complications in the pa- public hospitals of Tehran University of Medical
tients. Therefore, it is suggested that countries Sciences, Tehran, Iran from April 2007 to April
provide large scale screening programs for at risk 2008.
patients (4). Screening needs to establish accurate The study was approved by the Ethic Committee
and cost-effective tools and laboratory tests. Pol- of Tehran University of Medical Sciences.
ymerase chain reaction (PCR) has been success- Consecutive sampling was used. After signing an
fully used in research studies for the detection of informed consent, each participant completed a
Chlamydia trachomatis (CT) DNA. PCR is more questionnaire on demographic characteristics in-
sensitive than high quality cultures (5). This test is cluding age, education, occupation, gravidity, con-
expensive and needs more time but a previous traception and previous parities. Information about
study suggests that it is a promising method for infertility duration, type and etiology of infertility,
the detection of asymptomatic pelvic infection in history of abdominal surgeries, abortion or ectopic
patients with unexplained infertility (6). Enzyme pregnancy were also obtained and a physical ex-
linked immunosorbant assay (ELISA) can detect amination was conducted by a gynecologist. Up to
C. trachomatis antibodies as another diagnostic 15 ml of first catch urine (after not voiding urine
tool (7). for at least 2 hr) was collected into sterile contain-
Infection with C. trachomatis can cause urethri- ers without preservatives. The specimens were
tis, cervicitis, adnexitis, pelvic inflammatory dis- transported at room temperature for urine pro-
ease, or ectopic pregnancy (8) Subfertility (9) and cessing. Blood samples were obtained by veno-
infertility (10) in women. Most of these patients puncture and the serum was separated by centrifu-
are asymptomatic and are usually diagnosed with gingation and stored at −20°C.
the infection when they undergo infertility diag- Participants: Calculating an odds ratio to 1.7, the
nostic procedures (11). In some studies C. tra- prevalence of infection was estimated to be 35%
chomatis had greater prevalence in infertile than and 55% in fertile and infertile women, respec-
fertile women (12), but their prevalence was tively (15). We set the statistical significance level
shown to be the same in other studies (10, 11). at 0.05 and test power at 80% by comparative
A previous study reported that the molecular study. We determined the sample size 230 for
prevalence of C. trachomatis was 12.6% in wom- each group of participants. Finally, 234 infertile
an in Tehran, the capital of Iran (13), and in an- and 224 fertile women could complete the study.
other study it was 21.25% in women attending The first group included infertile women in their
Shahid Beheshti Hospital in Isfahan, Iran. Consid- childbearing age (18 to 49 years). Infertility de-
ering the different prevalence rates of C. tracho- fined as not being able to achieve pregnancy de-
matis infection in Iran, it is vitally essential to as- spite trying at least one year. Those with male
sess the impact of C. trachomatis on the reproduc- factor infertility and antibiotic therapy within 30
tive health of women (14). Most studies in Iran days before the assessment were excluded from
have been limited to case-series but case-control the study. The fertile group included women in
studies are so limited. The comparative preva- third trimester of pregnancy admitted to delivery
lence of Chlamydia is also one of the questions to room. In this group the exclusion criteria were
be answered in both fertile and infertile women. history of infertility, presence of genital tubercu-
We compare the prevalence of C. trachomatis losis, and recent antibiotic therapy.
infection in fertile and infertile women with both PCR: Urinary sediments were extracted after
PCR and ELISA methods in Tehran, Iran, during centrifugation at 5000 rpm for 20 min and frozen
April 2007 to April 2008. at −70°C in the laboratory of Children's Medical
We undertook this study as there seemed to be Center affiliated to Tehran University of Medical
limited studies on C. trachomatis prevalence in in- Sciences and they were subsequently transported
fertile patients in Iran. to Avicenna Research Institute for PCR.
DNA was extracted from the pellets as described

J Reprod Infertil, Vol 14, No 2, Apr-Jun 2013 68

JRI Effects of C. trachomatis on Fertility

by Sambrook and Russel and stored at −20°C cago IL, USA). A p-value less than 0.05 was con-
(16). sidered as statistically significant.
Amplification was performed by PCR method.
The primer sequences for the amplification of C. Results
trachomatis were as follow: DNA semi-nested or In this study, we recruited 234 infertile and 223
S: 5′-CTA-CGC-GTT-TGT-ACT-CCG-TCA-CA fertile women. The mean age of the infertile and
G-3′, anti-semi-nested or AS: 5′-AAC-TTA-TCC- the fertile groups were 29.85±6.26 and 26.85±
TCA-GAA-GTT-TAT-GCA-CTA -3`. PCR was 5.84 years, respectively. Infertility duration of the
performed in 25 µl volume of a master mix con- infertile women was 6.33±4.70 years and the
taining 1×PCR buffer (10 Mm Tris-HCl, pH=8.3, mean gravidity of pregnant women was 1.85±
50 mM KCl), 6 mM MgCl2, 0.2 µM of each pri- 1.08. The percentage of fertile women, with high-
mers, 0.6 mM of each dNTPs, 1.0 U Taq polymer- er education (57.4%) was greater than the infertile
ase, and 5 µl of the template DNA. Initial denatur- group (8.37%).
izing condition of this round was done at 94°C for Ovarian (101, 43.2%) and tubal (44, 18.8%)
5 min, 37 cycles of 30 s at 94°C, 30 s at 60°C, 30 causes of infertility were more frequent than other
s at 72°C and a final extension at 72°C for 5 min. causes of infertility. In 159 (67.9 %) women, the
The PCR product of 206 bp was electrophoresed type of infertility was primary. In the pregnant
and visualized on a 1.5% ethidium bromide stained group, 42 (18.8%) women had a previous history
agarose gel (16). of abortion and 94 (42.4%) had pervious parities.
PCR was performed on positive samples for 45 IgG about 21 (9.0%) infertile and 11 (5.0%) fer-
cycles, and semi-nested PCR on one of the nega- tile participants were positive for IgG (p=0.093).
tive samples to confirm the PCR in each series IgM was positive in 2 (0.9%) women with infertil-
(n=8). The second-round mixture contained the ity and 4 (1.8%) pregnant women (p=0.375) while
same components. Two µl of the first round PCR PCR was positive for C. trachomatis infection in
product was used as the template DNA for the 29 (12.4%) women with infertility and 19 (8.5%)
second-round amplification by using AS2: 5′- pregnant women (p=0.440). None of these differ-
GGT-AAT-AAT-TTG-CTG-GAT-GGC-3′ primers. ences were statistically significant.
The second-round amplification condition being In all the three diagnostic tests, C. trachomatis
the same as first-round. The PCR products were infection was not statistically significant between
loaded on a 1.5% gel stained with ethidum bor- primary and secondary infertility. IgG antibody
mide for electrophoresis. for C. trachomatis infection showed no statistical-
ELISA: C. trachomatis-specific IgG, and IgM ly significant differences between causes of infer-
were determined in serum using Sero CP-IgG, tility (p=0.340). However, PCR showed higher
-IgM protein ELISA; (EUROIMMUN, Germany), rates of infection among infertile women with
according to the manufacturer's instruction. Serum ovarian etiology (25.6%, p=0.002) than other eti-
was designated as positive if the cut-off index was ologies (Table 1).
greater than 1.1. ELISA was done in Avicenna After adjusting for possible confounding factors
Research Institute. in logistic regression analysis C. trachomatis posi-
Statistical Analysis: Diagnosis finding (IgG, IgM tivity was not statistically significant in infertile
and PCR) were compared between study groups against fertile women. The odds ratio was 1.499
using the chi-squared test. Moreover, chi-squared (0.611 to 3.679) for IgG, 0.440 (0.064 to 3.013)
was also used to compare C. trachomatis infection for IgM and 1.254 (0.613 to 2.562) for PCR. Sen-
between the cause and type of infertility test. Lo- Table 1. Positive results of tests based on causes of infertility
gistic regression was used to show association be- (n=234)
tween C. trachomatis infection and infertility. For
PCR IgG IgM
this analysis, positive results of each diagnostic
Uterus 1 (4.3%) 3 (12.5%) 0
test (IgG, IgM or PCR) were separately used as
Tubal 2 (4.9%) 4 (9.7%) 1 (2.3%)
dependent variables. Sensitivity, specificity, and
Ovarian 22 (25.6%) 4 (4.1%) 1 (1.0%)
positive and negative predictive values of ELISA
tests (IgG and IgM) were also determined. The Other 4 (7.0%) 9 (13.8%) 0
analyses were done by SPSS 13 (SPSS Inc, Chi- Total 29 (12.4%) 20 (8.7%) 2 (9.0%)

69 J Reprod Infertil, Vol 14, No 2, Apr-Jun 2013

 Hossein Rashidi B, et al. JRI
sitivity, specificity, positive and negative predic- ported the same prevalence for C. trachomatis
tive values, and accuracy for IgG results were infection in tubal and non-tubal etiologies for in-
6.3%, 92.5%, 10.7%, 87.3%, and 81.7%, respec- fertility (22).
tively; for IgM they were 2.1%, 98.5%, 16.7%, C. trachomatis infection had the same preva-
87.5%, and 86.4%, respectively. lence in primary and secondary causes of infertili-
ty in the present study. This result is in line with
Discussion study performed in Jordan (11); although there
Using different diagnostic methods, we found no were also some reports indicating greater preva-
significant differences between fertile and infertile lence for the infection in secondary than primary
women for C. trachomatis infection. Although infertility (12, 23). Having the same prevalence in
this finding is compatible with some studies (10, different types of infertility, it is probable that C.
11), but some other studies have shown greater trachomatis may induce infertility by other mech-
prevalence for C. trachomatis infection among in- anisms than tubal damage, opening the door for
fertile women and have mentioned it as an infertil- further investigations.
ity risk factor (12). In case-control studies, group An earlier study showed genital C. trachomatis
selection and control for confounding control can is very common (24). Educational programs about
explain parts of these differences. sexually transmitted diseases is a known way of
Prevalence of C. trachomatis in infertile women reducing the prevalence of these infections.
infection based on PCR and serologic detection of Enzyme-linked immunosorbent assay (ELISA) is
IgG and IgM respectively was 12.4%, 9.0% and the first generation of non-cultural tests to diag-
0.9%. In developing countries, this rate was re- nose chlamydial infection. ELISA uses an en-
ported to be 3.9% by PCR in Jordan (11) and zyme-linked monoclonal or polyclonal antibody
23.3% by direct immunoflurescence in Turkey directed at the C. trachomatis lipopolysaccharide
(17). About 24% of infertile women had a rate (25). In the presence of C. trachomatis, the anti-
lower than 10% in Western Europe. (18). These body binds to LPS, and the linked enzyme induces
studies showed that about 10% to 30% of infertile a change in color that can be detected by a spec-
woman had been infected by C. trachomatis Alt- trophotometer. One benefit of ELISA is that spec-
hough a rate of about 12.4% in the present study imens do not require refrigeration (25). In the pre-
is not indicative of a very high rate of infection, sent study ELISA showed low sensitivity but ac-
but it does not mean that the rate of C. tracho- ceptable specificity. Other researchers have also
matis infection is low in Iran. In this study, we reported low sensitivity (26) and adequate speci-
only evaluated patients in one of Tehran hospitals; ficity for the test (27). Therefore, ELISA can be
therefore, the results cannot be generalized. Preva- suggested as a screening test for detecting infec-
lence of C. trachomatis infection may be different tion in patients with infertility. For those who
in other areas in Iran, especially between rural and have a positive result for C. trachomatis infection
suburban areas. by this method, confirmatory tests are warranted.
These differences seem to be the result of differ- ELISA is also suggested for subgroups of patients
ences in study settings, such as duration of study, with endocervical, urethral, or conjunctival spec-
socioeconomic status, sample size and diagnostic imens (25).
methods. The sensitivity of PCR test for detecting C. tra-
Prevalence of C. trachomatis may also vary in chomatis in endocervical samples has ranged from
different groups of infertile women. There are 51.9% to 96.8% (28−30). PCR has a reported sen-
some reports that C. trachomatis infection is more sitivity of 44.4% to 82.5% (29, 30) for detecting C.
prevalent in tubal infertility than other types of trachomatis in urine samples from women. Speci-
infertility (15). Infection with C. trachomatis can ficity PCR for C. trachomatis for samples from all
cause adnexal adhesions and tubal obstruction reproductive organs has been reported to be 98.4%
(19) and it is the most common cause of tubal in- to 100% (30).
fertility (20). Therefore, it is rational to deduct All in all, ELISA is recommended as a screening
that the infection is more prevalent in tubal infer- test for detecting C. trachomatis infection in indi-
tility. Tubal assessment is recommended in infer- viduals suspected of the infection but a confirma-
tile women with a positive result for C. tracho- tory test needs to be done. Therefore, PCR can be
matis antibody (21). Our findings are compatible used as the confirmatory test for diagnosis of C.
with the study done in northern Iran, which re- trachomatis. Although nucleic acid amplification

J Reprod Infertil, Vol 14, No 2, Apr-Jun 2013 70

JRI Effects of C. trachomatis on Fertility

tests (NAATs) need more time and are more ex- 7. Numazaki K, Asanuma H, Niida Y. Chlamydia tra-
pensive but their accuracy and non-invasiveness chomatis infection in early neonatal period. BMC
are noticeable. Additionally, Quantitative PCR is Infect Dis. 2003;3:2.
more sensitive than PCR because it detects lower 8. Wagenlehner FM, Weidner W, Naber KG. Chla-
numbers of microorganisms. mydial infections in urology. World J Urol. 2006;
24(1):4-12.
Conclusion 9. den Hartog JE, Morré SA, Land JA. Chlamydia tra-
It seems that C. trachomatis detection and treat- chomatis-associated tubal factor subfertility: Im-
ment can be useful in infertile women improving munogenetic aspects and serological screening. Hum
their ART results. Due to the effects of chlamydia Reprod Update. 2006;12(6):719-30.
infection, tubal involvement and findings of this 10. Siemer J, Theile O, Larbi Y, Fasching PA, Danso
study, Chlamydia screening is highly suggested in KA, Kreienberg R, et al. Chlamydia trachomatis
infertile women before infertility management. Be- infection as a risk factor for infertility among
sides, prevention of maternal-fetal complications, women in Ghana, West Africa. Am J Trop Med
indicates C. trachomatis screening during preg- Hyg. 2008;78(2):323-7.
nancy. 11. Al-Ramahi M, Mahafzah A, Saleh S, Fram K.
Prevalence of Chlamydia trachomatis infection in
Acknowledgement infertile women at a university hospital in Jordan.
This project was supported by grant No. 840106- East Mediterr Health J. 2008;14(5):1148-54.
24 from Tehran University of Medical Sciences
and Avicenna Research Institute. 12. Malik A, Jain S, Hakim S, Shukla I, Rizvi M.
Chlamydia trachomatis infection & female inferti-
lity. Indian J Med Res. 2006;123(6):770-5.
Conflict of Interest
None of the authors had any conflict of interest. 13. Chamani-Tabriz L, Tehrani MJ, Akhondi MM, Mo-
savi-Jarrahi A, Zeraati H, Ghasemi J, et al. Chla-
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