Correspondence: Berna Seckin, MD,. G ü venlik Avenue, Yazanlar Street 28/6, A.Ayranc ı , Ankara, Turkey 06540. Tel: � 90 312 4272438. Fax: � 90 312 3124931. E-mail: bernaseckin1@hotmail.com

I N T R O D U C T I O N

Recurrent pregnancy loss (RPL) has been defi ned as three or more consecutive losses before 20 weeks of gestation or with a fetal weight of less than 500 g 1 . RPL is observed in about 2 – 4% of reproductive-age couples 2 . Various aetiologies have been proposed as contributing to RPL; these include genetic abnormalities, congenital

and acquired uterine anomalies, endocrine and autoim-mune diseases, thrombophilic disorders, and certain infections 3,4 .

In the literature, the prevalence of uterine defects, including various M ü llerian tract anomalies, endo-metrial polyps, submucous myomas and adhesions is high in women with RPL, ranging from 17 to 38%,

The European Journal of Contraception and Reproductive Health Care, October 2012; 17: 393–398

Offi ce hysteroscopic fi ndings in patients with two, three, and four or more, consecutive miscarriages Berna Seckin , Esma Sarikaya , Ayla Sarg ı n Oruc , Sevki Celen and Nedim Cicek

Department of Reproductive Endocrinology, Zekai Tahir Burak Women ’ s Health Education and Research Hospital, Ankara, Turkey

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

A B S T R A C T Objectives To assess hysteroscopic fi ndings in patients with two, three, and four or more, consecutive miscarriages, and to compare the prevalence of uterine abnormalities between women with different numbers of such miscarriages.

Methods Two hundred and sixty-fi ve women with two or more consecutive miscarriages were enrolled in the study. Patients were divided into three groups according to the number of their miscarriages: Group 1 (two miscarriages, n � 151), Group 2 (three miscariages, n � 69), and Group 3 (four or more miscarriages, n � 45). All participants underwent a diagnostic hysteroscopy. Congenital (arcuate uterus, septate uterus, unicornuate uterus) and acquired uterine abnormalities (intrauterine adhesions, polyp and submucous myoma) were recorded. The hysteroscopic results were compared between the groups.

Results No anomalies were detected in 152 patients (57%), whereas 43 (16%) had a septate uterus, 30 (11%) an arcuate uterus, three (1%) a unicornuate uterus, 18 (7%) intrau-terine adhesions, 17 (6 %) endometrial polyps, and two (1%) a submucous myoma. No signifi cant differences were found between the groups with regard to either congenital or acquired uterine abnormalities.

Conclusions Patients with two, three, and four or more consecutive miscarriages have a similar prevalence of uterine anatomical abnormalities. Diagnostic hysteroscopy should be carried out after two such miscarriages.

K E Y W O R D S Hysteroscopy ; Recurrent miscarriage ; Recurrent pregnancy loss ; Uterine anomalies

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

© 2012 The European Society of Contraception and Reproductive HealthDOI: 10.3109/13625187.2012.698767

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394 The European Journal of Contraception and Reproductive Health Care

depending on the type of the anomaly and the study design 5 – 7 . Hysteroscopy allows direct visualisation of the uterine cavity and it is an accurate screening tool for the diagnosis of uterine defects associated with RPL 8,9 . Congenital and acquired uterine anomalies can be treated hysteroscopically, resulting in improved outcomes 10 . For that reason, early diagnosis is critical. There is no specifi c number of pregnancy losses or fi rmly established criterion that mandates starting an evaluation of recurrent miscarriages. Many of the diagnostic tests have been recommended after three or more miscarriages. In recent years, most investiga-tors tend to offer a clinical evaluation in patients after two consecutive pregnancy losses 9,11,12 . However, data justifying this approach are scarce.

The purpose of this study was to investigate hystero-scopic fi ndings in women with two, three, and four or more consecutive pregnancy losses, and to compare the prevalence of uterine abnormalities in patients with different numbers of such miscarriages.

M E T H O D S

A prospective study was conducted from April 2009 through December 2011 in the Department of Reproductive Endocrinology of the Zekai Tahir Burak Women ’ s Health Education and Research Hospital, Ankara, Turkey. A miscarriage was defi ned as a spontaneous pregnancy loss up to 20 weeks ’ gesta-tional age. The expulsion of products of conception, the disappearance of fetal heart activity on ultrasound and the presence of a gestational sac with ß -hCG levels failing to rise were taken into consideration. Only women with two or more consecutive mis-carriages with the same partner were included. The study was approved by the Institutional Ethics Committee and informed consent was obtained from all participants.

Complete medical, obstetric and family histories were taken, and a physical examination was done. Basic diagnostic tests including full blood count, thyroid function tests, blood glucose level, and a pelvic ultra-sound were performed in all patients. In addition to these diagnostic tests, parental karyotypes were deter-mined and antiphospholipid antibodies (lupus antico-agulant and anticardiolipin antibodies) were measured in patients with three or more miscarriages as part of our clinical RPL research protocol, as recommended in the literature.

Molar pregnancies, ectopic pregnancies and induced abortions were not taken into account. Patients who had an abnormal karyotype, antiphospholipid syndrome or uncontrolled endocrine disorders were excluded. Women with acute or recent pelvic infection, suspected preg-nancy, or a diagnosis of cervical incompetence in previous pregnancies were also excluded from the study.

All participants meeting these criteria underwent a diagnostic hysteroscopy in the follicular phase of the menstrual cycle (between days 5 and 13) by either one of two of the authors of this study. All procedures were performed on an outpatient setting and without anaes-thesia (unless required for excessive pain), within a year after the last miscarriage. Use of a speculum to visualise the cervix or cervical grasping with a tenaculum was avoided. In the presence of a narrow cervical canal, 400 μ g misoprostol (Cytotec® 200 μ g tablets, Ali Raif, Istanbul-Turkey) was administered vaginally two hours before the procedure. In case the patient did not toler-ate the procedure paracervical block was performed or the procedure was rescheduled.

For the hysteroscopy, a 30 degree forward-oblique lens telescope and a 5 mm rigid hysteroscope (Karl Storz Endoscopy, Germany) with a single infl ow chan-nel were used. The hysteroscope was placed into the lower vagina and directed towards the cervix. Glycine 1.5% solution was used as a distending medium. On identifying the external ostium, the tip of the instru-ment was introduced into the cervical canal and guided into the uterine cavity. The hysteroscopy was consid-ered to have been successful if both tubal ostia were visualised. Hysteroscopic fi ndings were categorised as either being normal or showing congenital or acquired uterine anomalies. Congenital anomalies were classi-fi ed as arcuate uterus (showing a discrete bulging of the fundus towards the uterine cavity), septate uterus (with a septum more than 1 cm high), and unicornuate uterus . Intrauterine adhesions (characteristic of Asherman ’ s syndrome), endometrial polyps and submucous myomas were the acquired anomalies. No major complications occurred related to the hysteroscopies. In case a congenital anomaly was diagnosed, a complementary laparoscopic examination was offered.

Patients were divided into three groups according to the number of their consecutive miscarriages: Group 1 (two miscarriages), Group 2 ( three miscarriages) and Group 3 (four or more miscarriages). The prevalence of uterine anomalies diagnosed by hysteroscopy was compared between the groups .

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Hysteroscopy and consecutive miscarriages Seckin et al.

The European Journal of Contraception and Reproductive Health Care 395

Data were analysed by means of the Statistical Package for Social Sciences (SPSS) for Windows release 15.0 packet programme. Chi-square test and One-Way ANOVA test were employed to compare groups. For descriptive statistics, we resorted to frequencies and percentages for nominal data. Mean � Standard devia-tion (SD) and range (minimum-maximum) values were used for continuous data. Because the Chi-square test was repeated for multiple comparisons, the Bon-ferroni adjustment was applied. The level of statis-tical signifi cance was set at p � 0.05 and, with the Bonferroni adjustment, at p < 0.017.

R E S U L T S

We initially took into consideration 295 women with two or more consecutive miscarriages. Of these, four had an abnormal karyotype, fi ve an antiphospholipid syndrome, eight an uncontrolled endocrine disorder, seven a recent pelvic infection, and two a suspected pregnancy; they were therefore excluded. Four women with the diagnosis of cervical incompetence in preg-nancies in the past were also not enrolled. The study sample ultimately consisted of 265 patients who met all inclusion and exclusion criteria.

The mean age of the participants was 29.1 � 5.7 years (range 18 – 43 years). The number of previous pregnancies varied from two to eight (median: three). Of the 265 patients, 215 (81%) had no experience of a delivery before their consecutive pregnancy losses, 49 (19%) had delivered once, and one (0.4%) twice. The number of miscarriages varied from two to eight. One hundred and fi fty-one women (57%) had had two miscarriages (Group 1), 69 (26%) had had three

(Group 2), and 45 (17%) four or more miscarriages (Group 3). There was no statistical difference with regard to the previous delivery between the groups. The mean age of the patients was lower in Group 1 than in Groups 2 and 3 ( p � 0.029). Clinical charac-teristics of the groups are shown in Table 1.

Of the 265 participants, 152 (57%) had normal fi ndings at hysteroscopy, 76 (29%) had congenital anomalies, while 37 (14 %) had acquired anomalies. This is a more detailed account of the pathology identifi ed: 43 women (16%) had a septate uterus, 30 (11%) an arcuate uterus, three (1%) a unicornuate uterus, 18 (7%) intrauterine adhesions, 17 (6%) endo-metrial polyps, and two (1%) a submucous myoma. In all but one case, in which they were severe, the adhesions were discrete or moderately developed. The distribution of the hysteroscopic fi ndings between the groups is shown in Table 2.

There were no signifi cant differences between the three groups with regard to the prevalence of either congenital or acquired abnormalities ( p � 0.167). Also after Bonferroni correction for multiple testing, no statistically signifi cant differences were found between Groups 1 and 2, Groups 2 and 3, and Groups 1 and 3 ( p � 0.113, 0.203, and 0.027, respectively).

D I S C U S S I O N

Findings and interpretation

The present study shows that congenital or acquired uterine anomalies are present in a signifi cant proportion (43%) of women with recurrent miscarriages. The preva-lence of abnormal hysteroscopic fi ndings we detected

Table 1 Clinical characteristics of the groups.

Two miscarriages (Group 1) (n � 151)

Three miscarriages (Group 2) (n � 69)

Four or more miscarriages

(Group 3) (n � 45) p-value

Age (years) 28.6 � 5.7 (18 – 43)

28.9 � 5.9 (19 – 43)

31.2 � 5.02 (21 – 41)

0.029 ∗

Prior deliveries, n (percentage) and number of deliveries (range)

25 (17%) (0 – 1)

18 (26%) (0 – 2)

7 (16%) (0 – 1)

0.202

* p � 0.05 by One-Way ANOVA test.

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Hysteroscopy and consecutive miscarriages Seckin et al.

396 The European Journal of Contraception and Reproductive Health Care

in patients with two, three, and four or more, consecu-tive miscarriages was of a similar order of magnitude.

Strengths and weaknesses of the study

The strength of this study is that all hysteroscopies were done by only two examiners, who used the same cri-teria, so that inter-observer variation was minimalised. Yet our study has several limitations. Some of the patients did not accept a complementary laparoscopic examina-tion. We have been unable to determine whether laparoscopy provided any reliable information of value for establishing the diagnosis and for deciding on the therapeutic approach. Two other limitations are the lack of satisfactory data concerning reproductive outcomes of the patients after surgical treatment and clear diag-nostic criteria for the different types of anomalies.

Differences in results in relation to other studies

According to the medical literature the prevalence of developmental uterine anomalies is about three times greater in women with RPL and it varies between 6 and 38% 5 . In a large review by Saravelos et al . 7 , the prevalence of congenital anomalies was found to be 17%. The septate uterus is the most common congenital uterine anomaly and it is the malformation most fre-quently associated with poor pregnancy outcomes 13,14 . The role of the septate uterus as a cause of pregnancy

loss is due to a reduced intrauterine volume and inad-equate vascularisation for the developing embryo and placenta 13 . Although reduction of intrauterine volume is less in cases of arcuate uterus, it is also considered a signifi cant cause of RPL by many investigators 5,15 .

In the present study, the prevalence of congenital anomalies was higher than most commonly reported in the literature 7 . This could be due to the fact that our hospital is a referral centre where hysteroscopic evaluation of the uterine cavity is a common procedure for the patients with RPL. Uterine sep-tum was the most common congenital malforma-tion, which is consistent with other investigators ’ observations 8,16 .

Acquired anatomical abnormalities such as uterine myomas, polyps and adhesions can also be contributing causes of RPL 13 . The role of myomas and polyps in the genesis of recurrent miscarriages has been widely discussed. It has been suggested that the presence of these pathologies, especially submucous myomas can diminish blood fl ow and thus interfere with implanta-tion of the embryo 6,17 .

Intrauterine adhesions can result from curettage, intrauterine surgery or endometritis. Mechanisms by which adhesions can cause RPL include a diminished functional intrauterine volume and endometrial fi brosis 6 . In our study, intrauterine adhesions and polyps were the most frequently acquired anomalies (7% and 6%, respectively). Similar results have been reported by other authors 8,9 . In our series the

Table 2 Distribution of hysteroscopic fi ndings between the groups.

Findings

Group 1 Two

miscarriages (n � 151)

Group 2 Three

miscarriages (n � 69)

Group 3 Four or more miscarriages

(n � 45) Total

(n � 265) p-value

No abnormality 94 (62) 39 (57) 19 (42) 152 (57)Congenital anomaly 40 (27) 21 (30) 15 (33) 76 (29)Septate uterus 25 (17) 10 (15) 8 (18) 43 (16)Arcuate uterus 15 (10) 8 (12) 7 (16) 30 (11) 0.167 ∗

Unicornuate uterus 0 (0) 3 (4) 0 (0) 3 (1)Acquired anomaly 17 (11) 9 (13) 11 (24) 37 (14)Intrauterine adhesions 8 (5) 3 (4) 7 (16) 18 (7)Endometrial polyp 8 (5) 5 (7) 4 (9) 17 (6)Submucous myoma 1 (1) 1 (1) 0 (0) 2 (1)

Values are presented as number of patients with percentage in parentheses. ∗ p -value by Chi-square test.

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proportion of patients with intrauterine adhesions in the group with four or more miscarriages was higher than among those with two or three miscarriages (16% vs. 5% and 4%, respectively). This may be due to the fact that patients with four or more miscar-riages had undergone more curettages than women in the other groups.

Relevance of the fi ndings: Implications for clinicians

Uterine septum, intrauterine adhesions, polyps, myo-mas and fi broids are amenable to surgical correction. Consequently, many of these uterine anomalies, whether congenital or acquired, have a good repro-ductive prognosis 18,19 . Hysteroscopic metroplasty signifi cantly improves the subsequent reproductive outcome in women with recurrent miscarriages 14,20 . Giacomucci et al . 21 evaluated the term delivery rate after hysteroscopic surgery in patients with recurrent miscarriages and congenital uterine anomalies. In this retrospective case series it was found that the term delivery rate was about ten-fold higher after surgery. Treatment of acquired uterine abnormalities, such as adhesiolysis and the removal of submucous myomas can also lead to an improvement in the live-births pregnancy rates 18 .

An accurate diagnosis is a prerequisite for an ade-quate treatment. Post-abortion hysteroscopy is a simple and useful method for the diagnosis of uterine anoma-lies in patients with recurrent miscarriages 6,11,19,22,23 . Recently, there has been a tendency to investigate women after fewer miscarriages. Several authors have reported that they had found anomalies of the uterine cavity in patients with a history of two mis-carriages 8,9,11,12,24 . Our results are similar: congenital or acquired uterine anomalies were equally frequent in patients with two miscarriages compared with those who had suffered three, four or more miscarriages.

Offi ce hysteroscopy is a minimally invasive, highly accurate and effi cient diagnostic method in the detec-tion of uterine anomalies 8,19 . Carrying out the proce-dure in an outpatient setting without anaesthesia markedly reduces its cost. Hysterosalpingography, another low-cost but relatively uncomfortable diag-nostic tool, was not performed in our study as a fi rst line method of assessing the uterine cavity, because most of the patients recruited in this study were not

infertile. Ultrasound also is useful for assessment of uterine anomalies. However, there are no universally accepted criteria for the ultrasonographic diagnosis of congenital uterine anomalies and the value of these criteria remains unclear 7 . Laparoscopy allows direct visualisation of the contour of the uterus and offers the advantage of concurrent diagnosis and treatment. Therefore, we performed laparoscopy for the differential diagnosis of a septate or bicornuate uterus.

Unanswered questions and future research

There is no case-control study on record comparing live-birth rates in women who submitted to a surgical correction of their uterine abnormality with those of women with the same anomalies who did not. Recently, Sugiura-Ogasawara et al . 25 declared that 65 – 85% of patients with bicornuate or septate uterus have a successful pregnancy outcome after surgery. However, they have also stated that 59% of the patients have a good reproductive outcome without surgery, with a cumulative live-birth rate of 78%.

In a study by Christiansen et al . 26 , the usefulness of the investigations and treatments offered to women with RPL were evaluated from an evidence-based point of view. They reported a need for agreement concerning the thresholds for detecting what is abnormal and the importance of well-designed clinical studies evaluating the effi cacy of treatments was strongly emphasised. Finally, it is evident that prospec-tive randomised studies are required to assess the reproductive outcome in patients whose abnormalities have been surgically corrected in order to confi rm the value of carrying out the hysteroscopic evaluation after two consecutive miscarriages.

C O N C L U S I O N

According to our data the prevalences of uterine abnormalities among patients with two, three, and four or more consecutive miscarriages are similar. A diagnostic hysteroscopy should be contemplated after two such miscarriages.

Declaration of interest: The authors report no confl icts of interest. The authors alone are responsible for the content and the writing of the paper.

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