European Journal of Obstetrics & Gynecology and Reproductive Biology 156 (2011) 101104

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European Journal of Obstetrics & Gynecology and Reproductive Biology

journal homepage: www.elsevier.com/locate/ejogrb

Post-abortion hysteroscopy: a method for early diagnosis of congenital and acquired intrauterine causes of abortions
Ebru Cogendez, Zehra Nihal Dolgun *, Ilhan Sanverdi, Abdulkadir Turgut, Sadiye Eren
Zeynep Kamil Women and Childrens Health and Research Hospital, Turkey

A R T I C L E I N F O

A B S T R A C T

Article history: Received 26 February 2010 Received in revised form 25 November 2010 Accepted 24 December 2010 Keywords: Recurrent abortion Hysteroscopy Uterine anomalies

Objective: Recurrent pregnancy loss is often dened as three or more consecutive pregnancy losses but there are no strict criteria for initiation of investigations after a miscarriage. We compared the frequency of uterine anomalies diagnosed by hysteroscopy following one, two and three or more miscarriages. Study design: In our study 151 patients underwent diagnostic hysteroscopy following a missed or an incomplete abortion. Uterine septum, subseptum, arcuate uterus, and uterine hypoplasia are classied as congenital uterine anomalies and polyps, synechia, and submucous myomas are classied as acquired uterine abnormalities. Results: 151 Patients were enrolled in the study. The pregnancy numbers of the patients varied between 1 and 12. Sixty nine (46%) of the patients had one miscarriage, 42 (28%) had two miscarriages and 40 (26%) had three or more miscarriages. Diagnostic hysteroscopy revealed normal uterine cavity in 61.1% of the patients, congenital uterine anomalies in 20.4% and acquired uterine pathologies in 18.5%. Among the congenital anomalies, 14 (9.3%) were uterine septum, 10 (6.6%) were subseptate uterus, 4 (2.6%) were arcuate uterus and 3 (1.9%) were uterine hypoplasia. Among acquired abnormalities 14 (9.3%) were uterine synechia, 12 (7.9%) were endometrial polyps, and 2 (1.3%) were submucous myoma. Among patients who had one miscarriage 64.1% had a normal uterine cavity, 18.2% had congenital abnormalities and 17.7% had acquired uterine pathologies. Of patients with two miscarriages, 52% had a normal uterine cavity, 21.9% had congenital anomalies and 26.1% had acquired uterine pathology. In the three or more miscarriage group, 58.4% had normal uterine cavity, 25.3% had congenital anomalies, and 16.3% had acquired uterine pathology. We did not nd any statistically signicant difference between the number of miscarriages and pathologic diagnostic hysteroscopy ndings. Conclusions: Post-abortion ofce hysteroscopy is a simple and efcient tool in the early diagnosis of congenital and acquired uterine pathologies. Diagnostic hysteroscopy can be performed after the rst miscarriage in order to determine congenital and acquired uterine pathologies, with regard to the patients age and anxiety level. 2011 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Benign uterine pathologies such as mullerian anomalies, endometrial polyps, submucous myomas and synechias can cause miscarriages. Uterine abnormalities are classied according to their origins, e.g. congenital (mullerian anomalies) and acquired (submucous myomas, endometrial polyps and uterine synechias). Uterine septum is the most common congenital anomaly of the female reproductive tract, with an incidence of 2 3% in the general population. The spontaneous abortion rate is high, averaging approximately 65% of pregnancies in some studies [1].

Hysteroscopy is the gold standard for the evaluation of the endometrial cavity, since it enables direct visualization of the endometrium. Congenital and acquired uterine abnormalities can be detected and treated hysteroscopically, resulting in improved pregnancy outcomes [2]. There are no specic criteria to start investigation after miscarriage. The general approach to a patient with recurrent pregnancy loss is to start investigation after three or more miscarriages. In recent years, however, there has been a tendency to start investigation after two miscarriages [3]. Our aim in this study is to investigate the frequency of congenital and acquired uterine abnormalities in women suffering from miscarriages and their relation with the number of miscarriages. 2. Materials and methods

* Corresponding author at: F. Kerim Gokay Cd. Ceritler Ap. 232/28, Goztepe, Istanbul, Turkey. Tel.: +90 505 4502505; fax: +90 262 6582669. E-mail address: dr_nihaldolgun@hotmail.com (Z.N. Dolgun). 0301-2115/$ see front matter 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejogrb.2010.12.025

One hundred and fty-one patients who had miscarriages and afterwards underwent diagnostic hysteroscopy between October

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E. Cogendez et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 156 (2011) 101104 Table 1 Hysteroscopic ndings. Finding No abnormality found Congenital anomaly Arcuate uterus Septate uterus Subseptate uterus Hypoplasic uterus Acquired pathology Intrauterine adhesions Submucous myoma Endometrial polyp No. (%) 92 (61.1) 31 4 14 10 3 28 14 2 12 (20.4) (2.6) (9.3) (6.6) (1.9) (18.5) (9.3) (1.3) (7.9)

2005 and February 2007 were included in the study. Of these, 69 (46%) had one, 42 (28%) had two and 40 (26%) had three or more miscarriages during the rst 20 weeks of gestation. A miscarriage is dened as: the spontaneous expulsion of products of conception; the disappearance of fetal heart activity on ultrasound; a gestational sac which does not grow in consecutive weekly ultrasound examinations or a detected gestational sac with b hCG levels failing to rise in serial measurements. Of the 151 patients, 81 (53.6%) had a missed abortion, 29 (19.2%) an anembryonic pregnancy and 41 (27.1%) an incomplete abortion. Women were excluded if they were known to be carriers of balanced chromosomal abnormalities, had uncontrolled or previously diagnosed endocrine diseases such as diabetes or hypothyroidism, or had anti-phospholipid syndrome. We did not investigate the one- or two-miscarriage groups regarding endocrine disease or chromosomal abnormalities. In these groups, only detailed histories were taken and physical examination was done. For the three or more miscarriages group, chromosomal and endocrinological investigations were done, correlated with the literature. Patients who had any chromosomal or endocrine pathologies were excluded. Post-abortion diagnostic hysteroscopy was performed in 69 (46%) patients who had one miscarriage, 42 (28%) who had two, and 40 (26%) who had three or more miscarriages. We performed dilation and curettage (D&C) in all 69 (100%) patients in the onemiscarriage group. Of the 42 patients who had two miscarriages, 34 (80.9%) had two D&Cs and 8 (19%) had one. Of the 40 patients who had three or more miscarriages, 15 (37.5%) had four D&Cs, 10 (25%) had three D&Cs, 14 (35%) had two and one (2.5%) had one D&C. Regarding the D&C technique, 200 mcg misoprostol was administered before the procedure if it was needed for cervical ripening. The procedures were carried out at our gynecology clinic on an outpatient basis and without anesthesia. Each patient had pelvic examination and transvaginal ultrasonography before hysteroscopy. Hysteroscopy was performed at the end of rst menstrual bleeding following the miscarriage. Misoprostol (200 mcg) was administered vaginally to each patient 2 h before the procedure. The hysteroscopic procedure was performed in an ambulatory setting, using a rigid 5-mm hysteroscope (Olympus Optical, Germany). Isotonic solution was used as distension medium. The cervical canal and the whole uterine cavity were investigated by hysteroscopy to determine the type of abnormality. Uterine septum, subseptum, arcuate uterus and uterine hypoplasia are considered congenital uterine anomalies whereas polyps, synechia and submucous myomas are considered acquired uterine abnormalities. Semi-rigid operative hysteroscopic instruments such as grasping forceps and biopsy forceps were used for the treatment of small intrauterine lesions such as polyps and focal adhesions. Polyps, submucosal myoma and other suspicious lesions were biopsied for pathological examination. 2.1. Statistics Statistical Package for Social Sciences (SPSS) for Windows 10.0 program was used for descriptive data analysis. For qualitative

Table 2 The distribution of hysteroscopic ndings according to miscarriage numbers. Abortions (n) 1 2 3 and > No nding 44 (64.1%) 22 (52%) 23 (58.4%) Congenital anomaly 13 (18.2%) 9 (21.9%) 10 (25.3%) Acquired pathology 12 (17.7%) 11 (26.1%) 7 (16.3%) p

>0.05 >0.05 >0.05

data analysis, Chi-square, sensitivity and specicity tests were used. The results were interpreted as 95% condence intervals and a p < 0.05 signicance level. 3. Results The age of the patients varied between 18 and 42 years, with an average of 28.57 4.39 years. The number of previous deliveries varied from 0 to 2, with 108 patients (71.5%) having no previous deliveries, 24 (15.9%) one previous delivery and 19 (12.6%) having two previous deliveries. Of the 151 women, 31 (20.4%) had congenital anomalies while 28 (18.5%) had acquired pathology. Among all the patients, 92 (61.1%) had no pathological ndings on hysteroscopy. Hysteroscopic ndings are shown in Table 1. Fourteen patients (9.3%) had a septate uterus, 10 (6.6%) had a subseptate uterus, four (2.6%) had an arcuate uterus, three (1.9%) had uterine hypoplasia, 14 (9.3%) had intrauterine adhesions, 12 (7.9%) had polyps and two patients (1.3%) had submucosal leiomyoma. Patients were compared according to their miscarriage numbers, uterine pathology type and frequency. Among patients who had one miscarriage; 44 (64.1%) had a normal uterine cavity, 13 (18.2%) had congenital anomalies and 12 (17.7%) had acquired pathologies. Among those who had two miscarriages; 22 (52%) had a normal uterine cavity, 9 (21.9%) had congenital anomalies and 11 (26.1%) had acquired pathologies. In the three or more miscarriage group, 23 (58.4%) patients had a normal uterine cavity, 10 (25.3%) had congenital anomalies and 7 (16.3%) had acquired pathologies. There was no statistically signicant difference between the number of miscarriages and abnormal hysteroscopic ndings (p > 0.05) (Tables 2 and 3).

Table 3 The distribution of miscarriage cases according to hysteroscopy results. Hysteroscopy Uterine septum Endometrial polyp Submucous myoma Uterine synechia Total 1 Abortion n: 69 (45.7%) 4 5 0 4 13 (5.8%) (7.2%) (5.8%) (18.8%) 2 Abortions n: 42 (27.8%) 3 3 0 6 12 (7.1%) (7.1%) (14.3%) (28.6%) 3 and >abortions n: 40 (26.5%) 7 4 2 4 17 (17.5%) (10%) (5%) (10%) (23.5%) Total n: 151 (%) 14 12 2 14 42 (9.3%) (7.9%) (1.3%) (9.3%) (27.8%)

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4. Comments Nowadays the American Fertility Society classication is widely used for uterine malformations [4]. Uterine abnormalities can be diagnosed by a combination of ultrasound, hysteroscopy and/or laparoscopy. While mullerian anomalies can be diagnosed successfully using ultrasound, particularly three-dimensional ultrasound [57], hysteroscopy has the advantage in its ability to diagnose and treat intrauterine adhesions, broids and polyps. In this study we utilized conventional transvaginal ultrasonography and hysteroscopy for the detection of congenital and acquired uterine pathologies. We found 31 (20.4%) patients with congenital uterine anomaly and 28 (18.5%) with acquired uterine pathology. Ninety-two (61.1%) patients had no pathological hysteroscopic ndings. In 2008 Saravelos et al. reviewed studies from 1950 to 2007 and found the prevalence of congenital uterine anomalies was approximately 16.7% in the recurrent miscarriage population, 7.3% in the infertile population and 6.7% in the general population [8]. We found 31 (20.4%) congenital uterine anomales in our population. The septate uterus, according to the medical literature, is the most common congenital uterine anomaly, representing 50 80% of the mullerian alterations [9]. The conventional view of the mechanism of pregnancy loss with a uterine septum is that implantation into the poorly vascularized, brous septum leads to abnormal implantation or defective early embryonic development and subsequent abortion [1,10]. We found a uterine septum and subseptate uterus in 24 patients. They were the most frequent anomaly among patients with a congenital malformation in our study (77.4%). Proctor and Haney, using diagnostic laparoscopy, evaluated 35 patients with recurrent pregnancy loss and a split uterine cavity diagnosed by preoperative hysteroscopy or hysterosalpingography, and found that all the patients had uterine septum [11]. In the same study they declared that hysteroscopic septum resection accompanied by diagnostic laparoscopy is the appropriate approach. Saravelos et al. declared that hysteroscopy is a denitive diagnostic tool but is inadequate in differentiating between different anomaly types, so hysteroscopy with laparoscopy offers the advantage of type differentiation [8]. In our study, we preferred transvaginal ultrasonography instead of diagnostic laparoscopy as the differential diagnostic tool for the patients who had uterine septum suspected by hysteroscopy or hysterosalpingography. The cases that had a sole fundus on transvaginal ultrasound were diagnosed as uterine septum. Hysteroscopic septum resection is accompanied by a signicant improvement in the reproductive performance of the patients. Studies have shown that hysteroscopic resection of the septum in a septate uterus improves pregnancy outcome in subsequent pregnancies in women with recurrent miscarriages [1214]. Ventolini et al., in 2004, performed diagnostic hysteroscopy on patients who had three or more miscarriages and found 8.7% uterine septum, 21.8% intrauterine adhesions and 4.3% submucosal myoma [15]. The importance of uterine polyps and myomas in the genesis of abortion is widely discussed. The mere presence of one of them in the uterine cavity can interfere with implantation and fertility, creating a hostile environment to embryo implantation. It is estimated that about 41% of women with myomas, especially submucous ones, may abort [16,17]. Intrauterine adhesions due to excessive endometrial curettage may cause Ashermans syndrome, resulting recurrent pregnancy loss because of diminished intrauterine volume, endometrial brosis and inammation. In 1993 Friedler et al., using diagnostic hysteroscopy, evaluated 147 patients who had D&C after a rst trimester spontaneous abortion and found intrauterine adhesions (IUA) in 28 (19%) patients [18]. The incidence of IUA following only one abortion was 16.3% (16 out of 98 cases), all were of mild extent and lmy consistency,

occupying less than one-quarter of the uterine cavity. The incidence of IUA after two abortions was 14% (3/21) but the incidence after three or more spontaneous abortions was signicantly elevated (32%, 9/28). In our study, we found 14 (9.3%) IUA cases out of 151 patients. The distribution of IUAs was 4.3% (3/69) after one abortion, 14.2% (6/42) after two abortions and 12.5% (5/40) after three or more abortions. In 1996, Romer et al. performed postabortion hysteroscopy on 80 patients and found 17 (21.2%) patients with congenital uterine anomalies and 23 (28.8%) with acquired uterine pathology. In 40 (50%) patients there was no evidence of pathology by hysteroscopy [19]. In this study they found 10 septate uteri, 7 arcuate uteri, 20 IUA, 2 submucous myoma and 1 endometrial polyp. IUAs were statistically more common in patients with two or more abortions (27.8%) than in patients with one abortion (14.9%). Weiss et al. investigated retrospectively the frequency of congenital and acquired uterine pathologies in 165 patients who underwent postabortion diagnostic hysteroscopy [3]. Of the 165 women, 32 (19%) had congenital anomalies and 18 (11%) had acquired anomalies. One patient had both congenital and acquired anomalies. Among all the women, 116 (70%) had no pathological ndings on hysteroscopy. Among the patients who had two abortions, 15 (22%) had congenital anomaly and 8(12%) had acquired pathology and among the patients who had three or more abortions 17 (17%) had congenital anomaly and 11 (11%) had acquired pathology. The frequency or type of anomalies did not differ in patients with two miscarriages versus those with three or more miscarriages. In our study, when we compared hysteroscopic ndings with the number of miscarriages, we found the frequency of congenital anomalies was 18.2%, 21.9%, 25.3% and acquired pathologies was 17.7%, 26.1%, 16.3% for the patients who had one, two and three or more miscarriages respectively. There was no statistically signicant difference between congenital and acquired pathology frequency in three groups. Septate uterus, submucous myoma, polyps and intrauterine adhesions are surgically curable pathologies. In particular, hysteroscopic septum resection increases successful pregnancy rates from 320% to 7090% [20,21]. Hysteroscopic adhesiolysis also improves pregnancy outcome in women with recurrent miscarriages [22,23]. In our study we did not nd any statistically signicant difference between the frequencies of congenital and acquired uterine pathologies in the patients who had one miscarriage, two miscarriages or three or more miscarriages. Therefore performing hysteroscopy after one miscarriage will give the same uterine anomaly detection results as hysteroscopy after three miscarriages. Since ofce hysteroscopy is an easy-to-perform diagnostic procedure, the operator needs optimal experience. One should be able to investigate the cervical canal, the whole uterine cavity and the tubal ostia, and to diagnose any kind of pathology. For operative hysteroscopy, however, more experienced hands are essential. In recent years women have tended to become pregnant at older ages as they are taking active career roles. A miscarriage causes severe anxiety in those women who are conditioned to be successful in every eld including forming a family. They would like to know why and they demand treatment. As the early diagnosis and treatment of uterine anomalies affect pregnancy prognosis positively, performing hysteroscopy on even the onemiscarriage population makes sense. Hysteroscopy is an ofce procedure with complication risks similar to hysterosalpingography [24] but it has critical superiority in detecting uterine anomalies. Endocrinological tests and chromosomal investigations may be expensive and time-consuming procedures for the one- or two-miscarriage groups compared to the easy, ofce based,

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E. Cogendez et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 156 (2011) 101104 [12] Porcu G, Cravello L, DErcole C, et al. Hysteroscopic metroplasty for septate uterus and repetitive abortions: reproductive outcome. Eur J Obstet Gynecol Reprod Biol 2000;88:814. [13] Saygili-Yilmaz E, Yildiz S, Erman-Akar M, Akyuz G, Yilmaz Z. Reproductive outcome of septate uterus after hysteroscopic metroplasty. Arch Gynecol Obstet 2003;268:28992. [14] Valli E, Vaquero E, Lazzarin N, Caserta D, Marconi D, Zupi E. Hysteroscopic metroplasty improves gestational outcome in women with recurrent spontaneous abortion. J Am Assoc Gynecol Laparosc 2004;11:2404. [15] Ventolini G, Zhang M, Gruber J. Hysteroscopy in the evaluation of patients with recurrent pregnancy loss: a cohort study in a primary care population. Surg Endosc 2004;18(12):17824. [16] Buttram Jr VC, Reiter RC. Uterine leiomyomata: etiology, symptomatology and management. Fertil Steril 1981;36:43347. [17] Salvador E, Bienstock J, Blakemore KJ, Pressman E. Leiomyomata uteri, genetic amniocentesis, and the risk of second-trimester spontaneous abortion. Am J Obstet Gynecol 2002;186(5):9135. [18] Friedler S, Margalioth EJ, Kafka I, Yaffe H. Incidence of post-abortion intrauterine adhesions evaluated by hysteroscopya prospective study. Hum Reprod 1993;8(3):4424. [19] Romer T, Bojahr B, Muller J, Lober R. Early diagnosis of congenital and acquired intrauterine causes of abortion by post-abortion hysteroscopy. Geburtshilfe Frauenheilkd 1996;56(10):5425. [20] Homer HA, Li TC, Cooke D. The septate uterus: a review of management and reproductive outcome. Fertil Steril 2000;73:114. [21] Alborzi S, Dehbashi S, Parsanezhad ME. Differential diagnosis of septate and bicornuate uterus by sonohysterography eliminates the need for laparoscopy. Fertil Steril 2002;78(1):1768. [22] Goldenberg M, Sivan E, Sharabi Z, Mashiach S, Lipitz S, Seidman DS. Reproductive outcome following hysteroscopic management of intrauterine septum and adhesions. Hum Reprod 1995;10:26635. [23] Katz Z, Ben-Arie A, Lurie S, Manor M, Insler V. Reproductive outcome following hysteroscopic adhesiolysis in Ashermans syndrome. Int J Fertil Menopausal Stud 1996;41:4625. [24] Kupesic S. Clinical implications of sonographic detection of uterine anomalies for reproductive outcome. Ultrasound Obstet Gynecol 2001;18:387 400.

informative and see and cure option of hysteroscopy. These ndings support the idea of evaluating the uterine cavity by hysteroscopy especially in patients who had one or two miscarriages and cannot venture to lose another pregnancy. It is also encouraging that the ofce hysteroscopy is a minimally invasive procedure and easy to perform without anesthesia. References
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