Which infertile women should be indicated for sonohysterography?

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1 Ultrasound Obstet Gynecol 2004; 24: Published online in Wiley InterScience ( DOI: /uog.1721 Which infertile women should be indicated for sonohysterography? H. ANDO, S. TODA, M. HARADA, S. YOSHIDA, I. KONDO, T. MASAHASHI and S. MIZUTANI Department of Obstetrics and Gynecology, Nagoya University School of Medicine, Nagoya, Japan KEYWORDS: early pregnancy loss; endometrial polyp; infertility; sonohysterography ABSTRACT Objective To evaluate the indications for transvaginal saline contrast sonohysterography (TV-SCSH) in endometrial screening by transvaginal sonography in infertile women. Methods The study involved 850 consecutive infertile women presenting to an outpatient clinic. Using transvaginal ultrasound endometrial images were evaluated in the proliferative phase. Abnormal images were classified as follows: rugged (R), hyperechoic (H), waved (W), or thick (T). Clinical symptoms such as hypermenorrhea, dysmenorrhea and abnormal uterine bleeding were also recorded. Abnormal endometrial images were further evaluated on TV-SCSH. Age-matched women with normal endometrial images underwent TV-SCSH as controls. Results The endometrial pattern was abnormal in 111 patients (13.1%). Lesions that had been identified by TV-SCSH including endometrial polyps (44 cases), submucosal ta (29 cases), and intramural ta with mucosal extension (24 cases) were largely associated with the R and/or the H pattern, the W or the T pattern, and the W pattern, respectively. Sensitivity and specificity of the abnormal endometrial image for any lesion were 100% and 91.5%, respectively. Sixty-four patients (59.3%) were asymptomatic despite an abnormal endometrial image. Conclusions TV-SCSH should be performed on selected patients following assessment of endometrial images on transvaginal sonography in order to diagnose intra- and pericavitary lesions in infertile women. Copyright 2004 ISUOG. Published by John Wiley & Sons, Ltd. INTRODUCTION Certain types of uterine ta and endometrial polyps may be associated with implantation failure, early pregnancy loss or other adverse reproductive events 1. These uterine mass lesions are usually first recognized during routine observations on transvaginal sonography. However, small structural abnormalities can be missed on transvaginal ultrasound and differentiation between endometrial and myometrial abnormalities is not always possible 2. It has not been established how useful symptoms such as hypermenorrhea, dysmenorrhea and abnormal uterine bleeding are for indicating further examinations, because such lesions are sometimes asymptomatic. Transvaginal saline contrast sonohysterography (TV- SCSH) is a relatively simple, quick, safe, inexpensive and painless technique. It involves placing a catheter into the endometrial cavity and infusing a small amount of isotonic saline solution under sonographic visualization. TV-SCSH has been evaluated for symptomatic women with uterine ta 3, for perimenopausal women with irregular uterine bleeding 2,4 and for reproductive-aged women with at least two consecutive pregnancy losses 5, or abnormal uterine bleeding 6. TV-SCSH has been demonstrated to be as reliable as hysteroscopy to detect endometrial polyps 7,8 and submucosal ta 3. However, traditional hysterosalpingography as well as transvaginal sonography are not as reliable, especially for small masses 9. Although hysteroscopy (with direct biopsy) is a decisive diagnostic test for investigating intracavitary abnormalities, it does not offer enough information about myometrial or large endometrial masses. It is also noteworthy that hysteroscopy may occasionally be unsuccessful due to the inability to insert the hysteroscope and it may lead to inadvertent uterine perforation. Magnetic resonance imaging (MRI) would be an ideal diagnostic tool for precise mapping of large or moderate ta 10. However, MRI is only suitable for preoperative evaluation rather than routine use because of its relatively high cost. Correspondence to: Dr H. Ando, Department of Obstetrics and Gynecology, Nagoya University School of Medicine, 65, Tsurumai-cho, Showa-ku, Nagoya , Japan ( ando@med.nagoya-u.ac.jp) Accepted: 18 May 2004 Copyright 2004 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER

2 Infertility and SCSH 567 Since the report of Syrop and Sahakian 7 on 14 (13 asymptomatic) infertile women with endometrial polyps detected using TV-SCSH, there have been several papers on the use of TV-SCSH in infertile women, including those undergoing in-vitro fertilization 11 and intracytoplasmic sperm injection 12. The largest of these studies was by Hamilton et al. 13, involving 500 consecutive infertile women, in 58 (12%) of whom abnormalities were detected in 484 TV-SCSH examinations. They concluded that TV-SCSH was an acceptable first-line screening procedure for endometrial abnormalities in infertile women. However, it might be argued that all infertile women should not have routine TV-SCSH because only 12% had intracavitary lesions in this series. We have examined 850 consecutive infertile women using transvaginal sonography over a period of 6 years. For the current study we classified abnormal endometrial images into four patterns. The primary purpose of this study was to evaluate abnormal endometrial patterns on transvaginal sonography in infertile women to establish criteria for further screening with TV-SCSH. The secondary purpose was to analyze the supportive role of clinical symptoms such as hypermenorrhea, dysmenorrhea and abnormal uterine bleeding in the transvaginal sonography-based detection of uterine mass lesions. METHODS Between November 1995 and October 2001, a total of 850 consecutive infertile women were examined with transvaginal sonography at our infertility center. All the women had at least a 1-year history of infertility. All patients were examined during the first 7 days of their cycle, in the proliferative phase, with a Sonovista EX Model MEU-1581 (Mochida, Tokyo, Japan) ultrasound machine with a 7.5-MHz transvaginal probe. Initial sagittal and coronal ultrasound images of the uterus were obtained in all patients. When we set up the study, abnormal endometrial images on transvaginal sonography were classified into four patterns as illustrated in Figure 1. If the endometrial line was intermittent or there was localized distortion, the pattern was called rugged endometrial line (R). When there was a discrete hyperechoic area in or close to the endometrium, the pattern was referred to as hyperechoic region (H). If the endometrial line was smooth but not curved consistent with the version, the pattern was described as waved endometrial line (W). The double-layer endometrial thickness was determined on a mid-sagittal view, according to the method of Fleischer et al. 14, by measuring the distance between the anterior and posterior myometrial endometrial interfaces. A doublelayer thickness of > 12 mm was defined as thickening of the endometrium (T). All the abnormally appearing endometria were re-evaluated in the next menstrual cycle to exclude false-positive images such as mucus plugs and blood clots, unless the lesion was clearly visualized on the initial transvaginal ultrasound examination. (a) (d) (c) Figure 1 Schematic diagram showing endometrial image classification on transvaginal sonography. (a) Normal image. (b e) Abnormal images: (b) rugged endometrial line (R pattern); (c) hyperechoic region (H pattern); (d) waved endometrial line (W pattern); (e) thickening of the endometrium (T pattern). After obtaining informed consent, TV-SCSH was offered to the patients with abnormal endometrial images confirmed on transvaginal sonography. One hundred and seventy-six patients with normal endometrial appearance on transvaginal sonography were randomly chosen as controls. They were also examined with TV- SCSH for the purpose of tubal patency screening after giving consent. One hundred and eight age-matched controls were selected from the 176 women with normal endometrial pattern for comparison with the study group. The procedure was performed with the patient in the dorsal lithotomy position. A speculum was inserted into the vagina to expose the cervix and the external cervical os was cleansed with povidoneiodine solution. A balloon catheter (12-French Hyscath catheter; Sumitomo Bakelite, Tokyo, Japan) was advanced into the endometrial cavity through the cervical canal, and the balloon was filled with 1 ml saline. Pulling the balloon catheter slightly, approximately 10 ml sterile saline solution was slowly injected through the catheter under direct sonographic visualization. The average time for the TV-SCSH procedure per patient was 10 min. However, if a uterine lesion was suspected, it took significantly longer. The consideration for further diagnostic or therapeutic intervention was based on each individual clinical situation. Histological confirmation of the TV- SCSH diagnosis was available in those who underwent surgery including resectoscopy (n = 58). Transvaginal sonography and TV-SCSH were performed by seven board-certified gynecologists of the Japan (b) (e)

3 568 Ando et al. Society of Obstetrics and Gynecology (JSOG). To ensure quality control, all the ultrasound images were checked by at least two of the examiners to reach the final assessment diagnosis. For statistical analysis, Student s t-test or a two-tailed Fisher s exact probability test was used. The level of statistical significance chosen was P < RESULTS Clinical symptoms and endometrial images on transvaginal sonography During the study period, 111 patients (13.1%) had abnormal endometrial images on transvaginal sonography. Three patients declined examination by TV-SCSH despite the presence of the abnormal endometrial images. Thus, 108 cases of abnormal endometrial images and their age-matched control cases were included for further analysis. Patient characteristics of the two groups are summarized in Table 1. The number of patients with clinical symptoms, including hypermenorrhea, dysmenorrhea and abnormal uterine bleeding, was significantly higher in the abnormal pattern group. The difference was most conspicuous in those with abnormal uterine bleeding. However, the majority of the patients (59.3%) with abnormal images did not have any of the symptoms. Patterns of endometrial images on transvaginal sonography and TV-SCSH-based diagnoses Details of the abnormal endometrial patterns on transvaginal sonography and TV-SCSH-based diagnoses are summarized in Table 2. Representative abnormal images on transvaginal sonography and TV-SCSH of the same cases are shown in Figure 2. The R pattern (Figure 1b) and the H pattern (Figure 1c) were the most frequently observed in the polyp cases. However, six out of 11 cases without any lesion showed the R pattern. All six cases had a polypoid endometrium or what has been described as endometrial wrinkles or folds. The R pattern was accompanied by the H pattern in 28 cases, of which 25 cases had an endometrial polyp. The W pattern (Figure 1d) was frequently recognized both in the submucosal (n = 18/43; 41.9%) and the intramural (n = 24/43; 55.8%) cases. The T pattern (Figure 1e) was the typical pattern for the submucosal (n = 10/19; 52.6%) or the polyp (n = 6/19; 31.6%) cases. In our series, only one patient Table 1 Clinical details of the infertile patients with or without abnormal images on transvaginal sonography Image on transvaginal sonography* Abnormal Normal P Number of patients Mean (± SD) patient age (years) 33.5 ± ± Mean (± SD) duration of infertility (years) 6.0 ± ± No. of patients with Hypermenorrhea Dysmenorrhea Abnormal uterine bleeding Patients without these symptoms (n (%)) 64 (59.3%) 86 (79.6%) *Based on the classification into four abnormal patterns. Determined by Student s t-test. Determined by two-tailed Fisher s exact probability test. Some patients had more than one symptom. Table 2 Abnormal endometrial images on transvaginal sonography and transvaginal saline contrast sonohysterography (TV-SCSH)-based diagnoses TV-SCSH-based diagnosis (n) Ultrasound classification polyp Submucosal Intramural hyperplasia Negative lesion Total (n) Rugged (R) 33* 4* 0 0 6* 43* Hyperechoic (H) 34* 2* 0 1* 4* 41* Waved (W) 0 18* * Thick (T) 6* 10* 0 1* 1 19* Combined patterns R + H R + W R + T H + T T + W Total *Combined pattern is included. Two independent lesions were recognized in one patient.

Infertility and SCSH 569 Figure 2 Examples of the uterine images on

contrast sonohysterography (b, d, f, h).

(a) The R pattern. (b) Polypoid endometrium. (c) The H pattern.

sonography. No patient was found to have an endometrial carcinoma.

symptoms and TV-SCSH-based diagnoses in the cases with abnormal

4%) cases of submucosal were asymptomatic.

4 Infertility and SCSH 569 Figure 2 Examples of the uterine images on transvaginal sonography (a, c, e, g) and those on transvaginal saline contrast sonohysterography (b, d, f, h). Images on the left each correspond to the adjacent image on the right. (a) The R pattern. (b) Polypoid endometrium. (c) The H pattern. (d) polyp. (e) The W pattern. (f) Submucosal. (g) The T pattern. (h) Submucosal. was suspected of having endometrial hyperplasia on transvaginal sonography. No patient was found to have an endometrial carcinoma. Clinical symptoms and TV-SCSH-based diagnoses Table 3 shows clinical symptoms and TV-SCSH-based diagnoses in the cases with abnormal endometrial patterns on transvaginal sonography. In our series, 28 of 44 (63.6%) cases of endometrial polyp and 12 of 29 (41.4%) cases of submucosal were asymptomatic. In the patients with hypermenorrhea, submucosal ta were the most frequent finding (12/22; 54.5%). In patients who had abnormal uterine bleeding, the most frequent lesion was the endometrial polyp (6/12; 50.0%). Fiftyeight of 64 (90.6%) asymptomatic patients had polyp or, while only 6 of 64 (9.4%) asymptomatic patients had no lesions.

5 570 Ando et al. Table 3 Clinical symptoms and transvaginal saline contrast sonohysterography (TV-SCSH)-based diagnoses TV-SCSH-based diagnosis (n) Clinical symptom* polyp Submucosal Intramural hyperplasia No lesion Total (n) Hypermenorrhea Dysmenorrhea Abnormal uterine bleeding None Total *Some patients had two symptoms. Two independent lesions were recognized in one patient. Table 4 Transvaginal sonographic abnormality and intra- or pericavitary lesion detected on transvaginal saline contrast sonohysterography (TV-SCSH) TV-SCSH (n) Transvaginal sonography Lesion No lesion Abnormal* endometrial echo Normal* endometrial echo *Based on the classification into four abnormal patterns. Sensitivity: 100%. Specificity: 90.8% (95% CI, 85.6% 96.0%). Positive predictive value: 89.8% (95% CI, 84.1% 95.5%). Negative predictive value: 100%. Transvaginal sonographic abnormality and presence of any lesion In our 108 age-matched controls with normal endometrial pattern on transvaginal sonography, no lesion was detected on TV-SCSH. If we compare endometrial images on transvaginal sonography with TV-SCSH-based diagnosis as the gold standard, sensitivity of the transvaginal sonographic abnormality for any lesion was 100% and specificity was 90.8% (95% CI, 85.6% 96.0%) (Table 4). Positive and negative predictive values for any lesion were 89.8% (95% CI: 84.1% 95.5%) and 100%, respectively (Table 4). Lesions were confirmed by pathology in all cases that underwent surgery (n = 58; 53.7%). DISCUSSION Transvaginal sonography is a routine imaging tool for all patients attending an infertility outpatient clinic. We classified abnormal endometrial images during the proliferative phase on transvaginal sonography into four patterns to identify infertile patients for further screening of intra- and pericavitary lesions using TV-SCSH. The image classification allowed efficient identification of a select group for TV-SCSH although the classification alone could not reach the diagnosis of specific lesions. Clinical symptoms, including hypermenorrhea, dysmenorrhea and abnormal uterine bleeding, were not particularly helpful in identifying candidates for advanced analysis by TV-SCSH. The four abnormal endometrial patterns on transvaginal sonography were simple and easy to apply in clinical practice. No intra- or pericavitary mass lesions should be missed using this system. However, we cannot exclude the possibility of the potential bias that could result in a higher negative predictive value, since not all of the infertility patients with a normal transvaginal ultrasound examination had a TV-SCSH in our study. Specificity of the abnormal pattern was 90.8% in our analysis. The R and the H patterns covered 72.7% (n = 8) of the false-positive group (n = 11). Although we repeated endometrial imaging by transvaginal sonography in the subsequent menstrual cycle to avoid temporary retention of blood clots or mucus plugs, some other false-positive images such as shearing of normal endometrium could not be excluded. No cases of intrauterine synechiae or adhesions (IUAs) were recorded in our study. Salle et al. 15 reported that TV-SCSH is recommended in cases of suspected IUAs. Although IUAs may easily be suspected from a history of curettage as well as an apparent break on transvaginal sonography during the luteal phase, the detection of IUAs might be a limitation of our endometrial pattern classification. TV-SCSH has been most frequently indicated for the peri- or postmenopausal patients with abnormal uterine bleeding 2, With expansion of the technique into reproductive medicine, the indication for TV-SCSH has become complicated. In our series, the presence of abnormal uterine bleeding was significantly associated with the presence of a uterine lesion. However, those who had this symptom were only 10.3% (n = 10) of all abnormal cases with lesions (n = 97). Expanded symptom-based analysis including hypermenorrhea (n = 20) and dysmenorrhea (n = 15) also provided results of low sensitivity and specificity. It is of note that in 58 of 96 (60.4%) asymptomatic patients, ta or polyps could not have been identified if we had depended solely on the clinical symptoms. On the other hand, 22 (20.4%) asymptomatic patients had normal endometrial images on transvaginal sonography. TV-SCSH may provide additional information such as the location of a mass lesion in relation to the endometrial cavity, or the precise diagnosis. It can also offer useful information when considering mass resection based on the adverse effect on reproduction. In

6 Infertility and SCSH 571 conclusion, most infertility patients will have at least one transvaginal ultrasound examination at same point during their evaluation or treatment. Thus, determining when TV-SCSH is unnecessary would reduce costs, prevent treatment delay, and reduce patient inconvenience. ACKNOWLEDGMENTS We thank Dr Tomoko Ando, Dr Shin-ichiro Tsukahara, Dr Takayuki Moriwaki, Dr Kazunori Furugori, Dr Mikihiko Kato, Dr Noboru Yamahara, Dr Yasutaka Murata, Dr Yoshinari Katsumata, Dr Akira Iwase, Dr Shigeko Saito and Dr Toko Harata for clinical assistance. REFERENCES 1. Varasteh NN, Neuwirth RS, Levin B, Keltz MD. Pregnancy rates after hysteroscopic polypectomy and myomectomy in infertile women. Obstet Gynecol 1999; 94: Goldstein SR. Use of ultrasonohysterography for triage of perimenopausal patients with unexplained uterine bleeding. Am J Obstet Gynecol 1994; 170: Fedele L, Bianchi S, Dorta M, Brioschi D, Zanotti F, Vercellini P. Transvaginal ultrasonography versus hysteroscopy in the diagnosis of uterine submucous s. Obstet Gynecol 1991; 77: Goldberg JM, Falcone T, Attaran M. Sonohysterographic evaluation of uterine abnormalities noted on hysterosalpingography. Hum Reprod 1997; 12: Keltz MD, Olive DL, Kim AH, Arici A. Sonohysterography for screening in recurrent pregnancy loss. Fertil Steril 1997; 67: Laughead MK, Stones LM. Clinical utility of saline solution infusion sonohysterography in a primary care obstetricgynecologic practice. Am J Obstet Gynecol 1997; 176: ; Discussion: Syrop CH, Sahakian V. Transvaginal sonographic detection of endometrial polyps with fluid contrast augmentation. Obstet Gynecol 1992; 79: Cicinelli E, Romano F, Anastasio PS, Blasi N, Parisi C. Sonohysterography versus hysteroscopy in the diagnosis of endouterine polyps. Gynecol Obstet Invest 1994; 38: Soares SR, Barbosa dos Reis MM, Camargos AF. Diagnostic accuracy of sonohysterography, transvaginal sonography, and hysterosalpingography in patients with uterine cavity diseases. Fertil Steril 2000; 73: Dueholm M, Lundorf E, Hansen ES, Ledertoug S, Olesen F. Accuracy of magnetic resonance imaging and transvaginal ultrasonography in the diagnosis, mapping, and measurement of uterine s. Am J Obstet Gynecol 2002; 186: Kim AH, McKay H, Keltz MD, Nelson HP, Adamson GD. Sonohysterographic screening before in vitro fertilization. Fertil Steril 1998; 69: Alatas C, Urman B, Aksoy S, Mercan R, Nuhoglu A. Evaluation of uterine cavity by sonohysterography in women scheduled for intracytoplasmic sperm injection. Hum Reprod 1998; 13: Hamilton JA, Larson AJ, Lower AM, Hasnain S, Grudzinskas JG. Routine use of saline hysterosonography in 500 consecutive, unselected, infertile women. Hum Reprod 1998; 13: Fleischer AC, Kalemeris GC, Machin JE, Entman SS, James AE, Jr. Sonographic depiction of normal and abnormal endometrium with histopathologic correlation. J Ultrasound Med 1986; 5: Salle B, Gaucherand P, de Saint Hilaire P, Rudigoz RC. Transvaginal sonohysterographic evaluation of intrauterine adhesions. J Clin Ultrasound 1999; 27: Goldstein SR, Zeltser I, Horan CK, Snyder JR, Schwartz LB. Ultrasonography-based triage for perimenopausal patients with abnormal uterine bleeding. Am J Obstet Gynecol 1997; 177: O Connell LP, Fries MH, Zeringue E, Brehm W. Triage of abnormal postmenopausal bleeding: a comparison of endometrial biopsy and transvaginal sonohysterography versus fractional curettage with hysteroscopy. Am J Obstet Gynecol 1998; 178: Widrich T, Bradley LD, Mitchinson AR, Collins RL. Comparison of saline infusion sonography with office hysteroscopy for the evaluation of the endometrium. Am J Obstet Gynecol 1996; 174:

International Journal of Medical and Health Sciences

International Journal of Medical and Health Sciences Journal Home Page: http://www.ijmhrs.net ISSN:2277-4505 Original article Comparison Of Imaging Modalities In Abnormal Uterine Bleeding : Correlation