Septate Uterus: Detection and Prediction of Obstetrical Complications by Different Forms of Ultrasonography

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1 Septate Uterus: Detection and Prediction of Obstetrical Complications by Different Forms of Ultrasonography Sanja Kupesic, MD, PhD, Asim Kurjak, MD, PhD The aims of the study were to compare the accuracy of transvaginal ultrasonography, transvaginal color Doppler sonography, hysterosonography, and threedimensional ultrasonography in detection of septate uterus and to evaluate the occurrence of obstetrical complications in relation to septal dimension and vascularity. Each patient underwent transvaginal ultrasonography and color Doppler examination, whereas hysterosonography and three-dimensional ultrasonography were carried out in 76 and 86 patients, respectively. The sensitivity of different sonographic imaging modalities ranges between 95.21% and 99.29%. Color and pulsed Doppler sonographic studies of the septal area revealed vascularity in 71.22%. Patients with vascularized septa had a higher prevalence of obstetrical complications than those with avascularized septa (P < 0.05). Threedimensional ultrasonography and hysterosonography are highly accurate diagnostic tools for detection of uterine septa. We found no correlation between septal dimension and rate of obstetrical complications, although pregnancy loss was most likely to occur in patients with vascularized septa. KEY WORDS: Uterus, septate; Transvaginal color Doppler sonography; Hysterosonography; Threedimensional ultrasonography C ongenital uterine malformations are variable in frequency and usually are estimated to occur in 3 to 4% in general population, ABBREVIATIONS IVF, In vitro fertilization; AIH, Artificial insemination by husband; SPTA, Spatial peak temporal average; RI, Resistive index; HCG, Human chorionic gonadotropin; PPV, Positive predictive value; NPV, Negative predictive value; PSV, Peak systolic velocity; EDV, End diastolic velocity; IVF/ET, In vitro fertilization and embryo transfer Received April 1, 1998, from the Department of Obstetrics and Gynecology, Medical School, University of Zagreb, Sveti Duh Hospital, Zagreb, Croatia. Revised manuscript accepted for publication June 27, Address correspondence and reprint requests to Sanja Kupesic, MD, PhD, Department of Obstetrics and Gynecology, Medical School, University of Zagreb, Sveti Duh Hospital, Sveti Duh 64, HR Zagreb, Croatia. although less than half manifest clinical symptoms. 1 3 The frequency of symptomatic malformations is dominated by septate uterus (close to 50%) compared with other malformations. 3,4 Traditionally, septate uterus was diagnosed by x-ray hysterosalpingography or diagnostic hysteroscopy. More recently transvaginal ultrasonography was reported to be a sensitive tool for detection of uterine anomalies. 5,6 However, clear distinction between different types of abnormalities is difficult and operator dependent. 7,8 Lately, hysterosonography has been introduced. 9 This simple and minimally invasive approach permits the obtaining of anatomic images of endometrium and myometrium, accurate depiction of the septate uterus, and even the measurement of septal height and thickness. Three-dimensional ultrasonography also was reported to be a promising method for the assessment of uterine anatomy and diagnosis of congenital uterine anomalies by the American Institute of Ultrasound in Medicine J Ultrasound Med 17: , /98/$3.50

2 632 SEPTATE UTERUS J Ultrasound Med 17: , 1998 The objective of our study was to evaluate the accuracy of transvaginal ultrasonography, transvaginal color and pulsed Doppler sonography, hysterosonography, and three-dimensional ultrasonography in the preoperative diagnosis of septate uterus in patients with infertility. The second part of our study was attempted to evaluate the occurrence of obstetrical complications in relation to septal dimension and vascularity. MATERIALS AND METHODS A total of 420 infertile patients undergoing hysteroscopy during the 4 year period were included in this study. Table 1 summarizes intraoperative findings in the selected group of patients. The final diagnosis of the uterine disorder was confirmed by hysteroscopy and visualization of the peritoneal profile of the uterus by laparoscopy. The American Fertility Society classification of müllerian duct anomalies 11 was used to describe uterine defects. The criteria for diagnosis of an arcuate uterus were normal appearance of the cervix and myometrium, absence of fundal cleft, and a rounded appearance of the fundal portion of the uterine cavity. In cases of septate uterus, the proximal part of the uterine cavity was partially or completely divided by the septum. The fundal indentation, if present, had to be less than 1 cm in depth. When width of the septum exceeded 1 cm, the septum was considered thick. The diagnosis of bicornuate uterus was made by a visualization of the divergent cornua and large fundal cleft (> 1 cm). Among our patients, 278 patients had intrauterine septum corrected surgically. Fiftythree of the patients with septate uteri had a history of repeated spontaneous abortion, 121 had had one spontaneous abortion (96 in the first trimester, with 25 in the second trimester), 82 had primary sterility, Table 1: Intraoperative Findings in 420 Infertile Patients Undergoing Hysteroscopy Hysteroscopic Finding Number Submucous leiomyoma 46 Endometrial polyp 35* Intrauterine synechiae 19* Septate uterus 278 Arcuate uterus 28 Bicornuate uterus 16 Total 422 *One patient with endometrial polyp and one with intrauterine synechiae had an intrauterine septum. and 20 had premature delivery, including six patients with breech and two with transverse presentations. Forty-four of the patients with septate uterus underwent medically assisted reproduction: two patients with a history of repeated miscarriage had an IVF procedure, 14 IVF patients aborted spontaneously during the first trimester, six patients reported early spontaneous abortion after AIH procedure, three IVF patients had late abortions, and one IVF patient had a premature delivery with breech presentation. Furthermore, 18 patients with primary infertility and septate uteri underwent two or more IVF/ET procedures, which were unsuccessful owing to the presence of the male related or tubal factors, or both. Each patient underwent transvaginal ultrasonography and transvaginal color Doppler examination during the luteal phase of the cycle, when the endometrium is most prominent. A systematic examination of the uterine position, size, and morphologic characteristics was performed using 5 MHz transvaginal probe (Aloka 500, Aloka Corporation, Tokyo, Japan). With the use of B-mode transvaginal sonography, the morphology of uterus was carefully explored with emphasis to endometrial lining in both sagittal and transverse sections. The septum was visualized as an echogenic portion separating the uterine cavity into two parts. Once B-mode examination was completed by one sonographer (A.K.), transvaginal color Doppler examination was performed by another operator (S.K.), who was unaware of the previous finding. An Aloka SSD 2000 (Tokyo, Japan) equipped with a 5 MHz transvaginal probe for imaging and 6 MHz pulsed Doppler system for blood flow analysis was used. Pulse repetition frequency ranged from 2 to 42 KHz. The SPTA was approximately 80 mw/cm. Wall filters (50 Hz) were used to eliminate low-frequency signals. Color and pulsed Doppler interrogations were superimposed to visualize intraseptal vascularity. Flow velocity waveforms were obtained from all the interrogated vessels. For each recording, at least five waveform signals of good quality were obtained. During each procedure the RI was calculated automatically from the maximum frequency envelope as PSV minus EDV divided by PSV. The average duration of the procedure was 15 min. Instillation of isotonic saline solution (hysterosonography) was carried out in 76 patients during the follicular phase. All of these patients underwent endocervical culturing, and the results of culture affected the decision to perform the hysterosonogram either immediately or after the antibiotic therapy. Pregnancy was excluded by quantitative

3 J Ultrasound Med 17: , 1998 KUPESIC AND KURJAK 633 β-hcg assays before initiating the procedure. In these patients examination was performed on a gynecological table, and the uterine cervix was exposed with a speculum disinfected with iodine solution. A catheter with external diameter of 1.6 mm and internal diameter of 1.1 mm was introduced slowly into the cervix. The balloon was insufflated with 1.5 to 2 ml of sterile saline solution to avoid outflow of the fluid. A syringe containing 20 ml of isotonic saline solution was attached to the catheter and the fluid was injected slowly. For distention of the uterine cavity, approximately 10 to 20 ml of the contrast agent was required. The speculum was then withdrawn and the endovaginal probe introduced. Transverse and sagittal sections were carefully explored, and septum was visualized as an echogenic portion separating the uterine cavity into two parts. The sonologist who performed hysterosonography was unaware of the other tests findings. Eighty-six women undergoing hysteroscopy were examined by three-dimensional ultrasonography. All underwent transvaginal scanning and color and pulsed Doppler evaluation prior to the three-dimensional examination. Twelve of these patients underwent additional examination: instillation of the isotonic saline solution into the uterine cavity. The results of the previous diagnostic tests were not available to the ultrasonographer specialized for threedimensional ultrasonography. Three perpendicular planes of the uterus were displayed simultaneously on the screen, allowing a detailed analysis of the uterine morphology. The equipment used for threedimensional imaging was Combison 530 3D Voluson (Kretz Technik, Vienna, Austria). Three-dimensional sonographic volume was generated by the automatic rotation of the mechanical transducer through 360 degrees. 10 The acquired volume was in the shape of a truncated cone with a depth of 4.3 to 8.6 cm and a vertical angle α = 90 degrees. The medium acquisition time was 10 s. The obtained volumes were immediately stored on removable hard-disk cartridges (SyQuest 88 MB). The typical volume required 8 to 14 MB of memory. Stored information was then analyzed using computer-generated planar reformatted sections. Frontal reformatted sections were particularly useful for detection of the uterine abnormalities. The patients undergoing additional examination (hysterosonography or three-dimensional ultrasonography, or both) were chosen at random. The protocol was approved by the Ethics Committee of the hospital, and each patient gave written informed consent. All the results were related to the findings at hysteroscopy, and for each technique specificity, sensitivity, positive predictive value, and negative predictive value were expressed. Fisher s exact test was used as appropriate; P < 0.05 was considered statistically significant. RESULTS Table 2 summarizes the sensitivity, specificity, positive predictive value, and negative predictive value of transvaginal sonography, transvaginal color and pulsed Doppler ultrasonography, hysterosonography, and three-dimensional ultrasonography for the diagnosis of septate uterus. In 264 cases septate uterus was suspected by transvaginal ultrasonography, whereas 14 patients were reported to have normal finding and were expressed as representing false-negative results. Therefore, the sensitivity of transvaginal sonography in the diagnosis of septate uterus was 95.21%. Transvaginal color and pulsed Doppler sonography enabled the diagnosis of septate uterus to be made in 276 cases, reaching a sensitivity of 99.29%. In one patient with endometrial polyp and one with intrauterine synechiae, septate uteri were not correctly diagnosed. Therefore, the reliability of color and pulsed Doppler examination was reduced if other intracavitary structures (such as intrauterine synechiae, endometrial polyp, or submucous leiomyoma) were present. Color and pulsed Doppler studies of the septal area revealed vascularity in 198 (71.22%) patients (Fig. 1). The RI values obtained from the septum ranged from 0.68 to 1.0 (mean RI, 0.84 ± 0.16) (Fig. 2). Eighteen patients demonstrated absence of diastolic blood flow, whereas in the rest a continuous diastolic flow was present. Table 2: Sensitivity, Specificity, PPV, and NPV of Various Imaging Modalities for the Diagnosis of Septate Uterus* Imaging Sensitivity Specificity PPV NPV modality (%) (%) (%) (%) Transvaginal sonography Transvaginal color Doppler sonography Hysterosonography Three-dimensional ultrasonography *420 patients with history of infertility or recurrent abortions, or both.

4 634 SEPTATE UTERUS J Ultrasound Med 17: , 1998 Figure 1 Transvaginal scan demonstrates septate uterus. Note two separate endometria (arrows) in the proliferative phase of the menstrual cycle. Color Doppler sonography exposes vessels supplying the uterine septum. Figure 2 In the same patient as in Figure 1, color signals explored by pulsed Doppler waveform analysis (right) show moderate to high resistance blood flow (RI = 0.65) typical of radial arteries. Hysterosonography, which was carried out in 76 patients, reached 100% specificity and positive predictive value. In one patient with extensive intrauterine synechiae, hysterosonography did not detect a intrauterine septum, although it was successful in diagnosing septate uterus in the remaining 54 patients. Good quality three-dimensional images were obtained in 86 patients (Fig. 3). The sensitivity and specificity of three-dimensional ultrasonography were 93.38% and 100%, respectively. A false-negative result in one patient was caused by a fundal fibroid distorting the uterine cavity. Three-dimensional ultrasonography therefore correctly detected septate uterus in 61 patients. Interestingly, in our study septate uterus was not mistaken for bicornuate uterus when transvaginal color Doppler sonography, hysterosonography, and three-dimensional ultrasonography were performed. However, in one patient with bicornuate uterus transvaginal ultrasonography misinterpreted septate uterus. The second part of our study evaluated the rate of obstetrical complications in relation to septal dimension and vascularization (Table 3). We found no correlation between septal height and occurrence of obstetrical complications (P > 0.05). In other words, abortions and late pregnancy complications occurred with the same rate in patients with small septa that divided less than one third of the uterine cavity (86 of 126) and those with division of more than two thirds of the uterine cavity (108 of 152). The same was true of septal thickness: obstetrical complications were found in the same proportion of the patients with thin (64 of 92) and those with thick septa (130 of 186) (P > 0.05). Indeed, previous obstetric performance correlated significantly with septal vascularity. Patients with vascularized septa had significantly higher prevalence of early pregnancy failure and late pregnancy complications (169 of 198) than those with avascularized septa (25 of 80) (P < 0.05). DISCUSSION Until now clinicians have had to perform at least two procedures to rule out the diagnosis of the septate uterus. The gynecologist should be aware that long diagnostic evaluation delays the treatment and increases the cost, patient discomfort, and risk associated with each of the diagnostic procedures. 9 Our study clearly demonstrates that transvaginal ultrasonography can assess uterine morphology precisely, including the endometrial lining and outer contour of the uterine muscle. Three-dimensional ultrasonography permits the obtaining of planar reformatted sections through the uterus, which allow precise evaluation of the fundal indentation and the length of the septum. 10 Based on our experience, this technique may give a wrong impression of an arcuate uterus in patients with a fundal leiomyoma. In such cases the uterine cavity has a concave shape, while fundal indentation is more subtle. Furthermore, shadowing caused by uterine fibroids, irregular endometrial lining, and decreased volume of the uterine cavity (in cases of

5 J Ultrasound Med 17: , 1998 KUPESIC AND KURJAK 635 Figure 3 Three-dimensional scan of a septate uterus that is characterized by a normal outer uterine contour and thick septum extending into the uterine cavity. intrauterine adhesions) are obvious limitations of three-dimensional ultrasonography. Color Doppler technique facilitates the visualization of the myometrial portion of the uterus by enhancing the detection of the radial arteries. Color and pulsed Doppler interrogation revealed septal vascularity in 71.22% of the patients, revealing that most of the septa consisted of myometrial vessels. The same results were obtained by Dabirashrafi and coworkers, 12 who performed a histologic study of the uterine septa from 16 patients undergoing abdominal metroplasty. Four specimens were taken from the uterus in each case: from the septum near the serosal layer, at the midpoint of the septum, at the level of the tip of the septum, and from the left posterior aspect of the uterus away from the septum. Statistical Table 3: Rate of Obstetrical Complications Relating to Septal Morphology and Vascularity Septal Obstetrical Characteristics Complications N (%) N (%) Significance Height Partial septum 126 (45.32) 86 (68.25) P > 0.05 Complete 152 (54.68) 108 (71.05) septum Thickness < 1 cm (thin) 92 (33.09) 64 (69.56) P > 0.05 > 1 cm (thick) 186 (66.91) 130 (69.89) Vascularity Vascularized 198 (71.22) 169 (85.35) P < 0.05 Avascular 80 (28.78) 25 (31.25) analysis for multiple comparisons revealed that septa contained less connective tissue than other features such as muscle tissue, muscle interlacing, and vessels with a muscle wall. The results obtained by Dabirashrafi and colleagues is contradictory to the findings of March 13 and Fayez, 14 who found that the septum is composed of fibroelastic tissue with fewer muscle fibers. Classic theory proposed that the connective tissue in the septum causes poor decidualization and placentation at the implantation site. 13,14 Results presented in our study demonstrate that patients with vascularized septa had a significantly higher rate of obstetrical complications than those with avascularized septa. Therefore, we can postulate that obstetrical complications are caused by the higher and uncoordinated activity of muscular tissue. Although both twodimensional and three-dimensional imaging are accurate in detection of the uterine anomalies, color Doppler imaging has a potential to predict likelihood of early pregnancy failure and obstetrical complications in patients with septate uterus. Potentially, this technique may help to select which patients actually need the therapeutic hysteroscopic procedure. However, this should be studied in a randomized controlled fashion, which we are performing at present in our Department. Septal incision seems to eliminate an unsuitable site of implantation through revascularization of the connective fundal tissue and elimination of the unfavorable uterine contractions. Since both of these events can be detected by color and pulsed Doppler ultrasonography, this technique can be efficiently used for follow-up of the patients who underwent operative hysteroscopy. REFERENCES 1. Ashton D, Amin HK, Richart RM, et al: The incidence of asymptomatic uterine anomalies in women undergoing transcervical tubal sterilization. Obstet Gynecol 72:28, Sorensen S: Estimated prevalence of müllerian anomalies. Acta Obstet Gynecol Scand 67:441, Gaucherand P, Awada A, Rudigoz RC, et al: Obstetrical prognosis of septate uterus: A plea for treatment of the septum. Eur J Obstet Gynecol Reprod Biol 54:109, Fedele L, Arcaini L, Parazzini F, et al: Metroplastic hysteroscopy and fertility. Fertil Steril 59:768, Valdes C, Malini S, Malinak LR: Ultrasound evaluation of female genital tract anomalies: A review of 64 cases. Am J Obstet Gynecol 149:285, Nicolini U, Bellotti B, Bonazzi D, et al: Can ultrasound be used to screen uterine malformation? Fertil Steril 47:89, 1987

6 636 SEPTATE UTERUS J Ultrasound Med 17: , Reuter KL, Daly DC, Cohen SM: Septate versus bicornuate uteri: Errors in imaging diagnosis. Radiology 172:749, Randolph J, Ying Y, Maier D, et al: Comparison of real time ultrasonography, hysterosalpingography, and laparoscopy/hysteroscopy in the evaluation of uterine abnormalities and tubal patency. Fertil Steril 5:828, Salle B, Sergeant P, Galcherand P, et al: Transvaginal hysterosonographic evaluation of septate uteri: A preliminary report. Hum Reprod 11:1004, Jurkovic D, Geipel K, Jauniaux E, et al: Three dimensional ultrasound for the assessment of uterine anatomy and detection of congenital anomalies: A comparison with hysterosalpingography and two dimensional sonography. Ultrasound Obstet Gynecol 5:238, American Fertility Society: The American Fertility Society classifications of adnexal adhesions, distal tubal occlusion, tubal occlusion secondary to tubal ligation, tubal pregnancies, müllerian anomalies and intrauterine adhesions. Fertil Steril 49:944, Dabirashrafi H, Bahadori M, Mohammad K, et al: Septate uterus: New idea on the histologic features of the septum in this abnormal uterus. Am J Obstet Gynecol 172:105, March CM: Hysteroscopy as an aid to diagnosis in female infertility. Clin Obstet Gynecol 26:302, Fayez JA: Comparison between abdominal and hysteroscopic metroplasty. Obstet Gynecol 68:399, 1986