The characterization of common ovarian cysts in premenopausal women

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1 Ultrasound Obstet Gynecol 2001; 17: The characterization of common ovarian cysts in Original Blackwell Paper Science, Ltd premenopausal women K. JERMY, C. LUISE and T. BOURNE Gynaecological Ultrasound and Minimal Access Surgery Unit, Department of Obstetrics & Gynaecology, St George s Hospital Medical School, London, UK KEYWORDS: Dermoid, Endometrioma, Pattern recognition, Transvaginal ultrasonography ABSTRACT Objectives The evaluation of the predictive value of transvaginal ultrasound in the assessment of benign adnexal pathology in premenopausal women, based on the recognition of characteristic morphologic patterns particular to endometriotic and dermoid ovarian cysts. Methods This was a prospective study. All premenopausal women undergoing surgery for a suspected ovarian cyst underwent a transvaginal ultrasound examination in the week prior to surgery. Between June 1997 and January 2000, 132 women underwent surgery for a suspected ovarian endometrioma or dermoid cyst. The endpoints were either the direct visualization of the cyst wall and contents at surgery, or the histologic evaluation of removed tissues. Results Of 83 suspected endometriomas (11 bilateral), 80 were confirmed at surgery and of 68 suspected benign cystic teratomas (eight bilateral), 66 were confirmed by histology. The positive predictive value of transvaginal ultrasonography for the diagnosis of endometrioma and dermoid cysts was 96.4% and 97.1%, respectively. The false positive rates were 3.8% and 3.0%, respectively. There were no malignancies in either group. Conclusions Based on the recognition of characteristic ultrasound patterns alone, the positive predictive value of transvaginal ultrasonography for the diagnosis of these common, benign cysts in premenopausal women is very high and can be used reliably to select women for appropriate surgery. INTRODUCTION The prevalence of adnexal pathology among young women is high and the overwhelming majority of these lesions will be benign in nature. The ability to discriminate accurately between benign and malignant disease of the ovary preoperatively allows appropriate management, whether expectant, under the care of the gynecologic oncologist or using minimal access surgical techniques. A large proportion of benign ovarian cysts will be functional in nature and if asymptomatic can be managed expectantly, avoiding the need for surgery. When surgery is required, the vast majority of benign adnexal masses can be treated using minimal access surgical techniques. Laparoscopy, compared with laparotomy, has been shown to reduce hospital stay, postoperative morbidity and recovery period, without increasing the risk of spillage of the cyst contents 1. Appropriate case selection is imperative for successful laparoscopic surgery; accurate preoperative assessment is pivotal. Cases likely to involve advanced surgical techniques, such as stage IV endometriosis or complex ovarian cysts, should be managed by appropriate centers. Transvaginal ultrasonography has an established role in the evaluation of adnexal masses. It provides an accurate assessment of ovarian morphology and is a significant contributor to mathematical models being developed to assess ovarian tumors 2,3. There are several types of ovarian cyst that can be assessed using the recognition of characteristic morphologic patterns. Endometriomas 4,5 and dermoid cysts 6 are two examples, accounting for over two-thirds of persistent adnexal masses in premenopausal women 7. These lesions can be particularly difficult to score using morphologic scoring systems and as angiogenesis is ubiquitous throughout the ovarian cycle, color Doppler is of limited value 8. Accurately identifying this subset of benign lesions will allow us to concentrate on the characterization of other, more difficult lesions. This may enhance our ability to differentiate between benign and malignant tumors more effectively using transvaginal ultrasonography. The aim of this study was to demonstrate the predictive value of the subjective interpretation of ultrasound for the assessment of benign adnexal pathology in premenopausal women, based on the recognition of characteristic features particular to endometriotic and dermoid cysts. Correspondence: Dr K. Jermy, Department of Obstetrics & Gynaecology, St George s Hospital Medical School, Cranmer Terrace, London SW17 0RE, UK ( kjermy@aol.com) Received , Revised , Accepted ORIGINAL PAPER

2 METHODS Between June 1997 and January 2000, 60 premenopausal women underwent surgery for a total of 68 suspected dermoid cysts (eight bilateral) and 72 premenopausal women underwent surgery for 83 suspected endometriotic cysts (11 bilateral). Their mean ages were 32 years (range years) and 33 years (range years), respectively. A transvaginal ultrasound scan was performed in all women undergoing surgery for a suspected endometrioma or benign cystic teratoma. This was performed within a week of surgery by one experienced operator (T.B.), using a 5-MHz transducer for B mode imaging (Aloka SSD 2000; Aloka Co., Tokyo, Japan). The uterus and subsequently the adnexae were imaged in both coronal and sagittal planes. A complete morphologic evaluation of the mass was made. A subjective assessment of the type of ovarian cyst was then made. An endometrioma was suspected by the presence of a thickwalled, cystic structure containing homogeneous, low-level echoes. This appearance of the cyst fluid is often described as being ground glass in character (Figures 1 and 2). In comparison, the ultrasound characteristics of dermoid cysts are highly variable, ranging from predominantly cystic to uniformly dense. The most distinctive feature is the presence of a discrete highly echogenic focus, with posterior shadowing (Rokitansky protuberance). Other characteristics considered pathognomonic are fine, echogenic bands (representing hair) within the cystic area and the presence of a fat fluid level 6,9,10 (Figures 3 and 4). The endpoints were either the histologic evaluation of removed tissues, or in the case of endometriomas, the direct visualization of the internal wall of the cyst and its contents intraoperatively (Figure 5). The positive predictive value and false positive rates were calculated for each group of masses separately. No data were available regarding false negative cases. As a result of this, the sensitivity and negative predictive values could not be calculated for this population of women. Figure 1 Large ovarian endometrioma. Thick walled cystic structure containing homogeneous ground-glass contents. Figure 3 Benign cystic teratoma: large cystic component, containing fine, echogenic strands, also with a smooth, hyperechogenic solid area (Rokitansky protuberance). Figure 2 Bilateral ovarian endometriomas kissing in the midline behind the uterus. Figure 4 Benign cystic teratoma: large echodense area with posterior acoustic shadowing. Ultrasound in Obstetrics and Gynecology 141

3 Table 2 Details of false positive endometrioma data Figure 5 Laparoscopic view of the internal pseudocapsule of an ovarian endometrioma after drainage of the cyst contents, prior to electro/laser ablation. Sonographic findings 15-year-old presenting with abdominal pain. Unilocular cystic structure arising from the pelvis with a volume of 1016 ml and ground glass echogenic contents 39-year-old para 2 presenting with pelvic pain. Unilocular cyst with a volume of 135 ml and an irregular internal wall with ground glass contents 25-year-old para presenting with pelvic pain. 278 ml unilocular cyst with an irregular internal wall and ground glass cyst contents Histology Aganglionic bowel (Hirschprung s) Hemorrhage fimbrial cyst Hydrosalpinx adherent to bowel Table 1 Predictive value of transvaginal ultrasonography for the diagnosis of endometriomas and dermoids Ultrasound diagnosis Endometrioma Dermoid True positives False positives 3 2 Positive predictive value, % False positive rate, % Table 3 Details of false positive dermoid data Sonographic findings 35-year-old para 0 presenting with acute pelvic pain. Unilocular cyst of mixed echogenicity with a volume of 59 ml and an irregular internal wall 50-year-old para 2 presenting with chronic pelvic pain. Septated ovarian cyst of mixed echogenicity with a volume of 21 ml Histology Edematous fibrothecoma Fimbrial cyst RESULTS Statistical outcomes One hundred and thirty-two women underwent surgery over the study period for a suspected endometrioma or dermoid cyst. Of 83 suspected endometriomas, 80 were confirmed at surgery and of 68 suspected benign cystic teratomas, 66 were confirmed histologically. There were no malignancies in either group. The positive predictive value of transvaginal ultrasonography for the diagnosis of endometrioma and dermoid cysts was 96.4% and 97.1%, respectively. The false positive rates were 3.8% and 3.0%, respectively (Table 1). Tables 2 and 3 summarize the ultrasonographic, clinical and histologic findings of the five false positive cases. Population demographics The demographic characteristics of the women undergoing surgery are summarized in Table 4. Over 70% of the population in both groups were nulliparous. In five patients a suspected endometrioma was detected during routine antenatal ultrasound screening. Ultrasound confirmed the persistence of the cyst postnatally and surgery was undertaken at this stage. These accounted for all the asymptomatic cases within the endometrioma group. Ultrasonography during early pregnancy also detected the majority of asymptomatic cysts Table 4 Characteristics of the 132 patients undergoing surgery within the dermoid group. One patient required surgery during early pregnancy for a symptomatic dermoid cyst. Surgical intervention Dermoids n = 60 (%) Endometrioma n = 72 (%) Age (mean) years Nulliparity 43 (72) 54 (75) Presenting complaint Menstrual disturbance 15 (25) 21 (29) Dysmenorrhea 4 (6) 29 (40) Acute pelvic pain 7 (12) 3 (4) Chronic pelvic pain 17 (28) 21 (29) Dyspareunia 1 (2) 7 (10) Infertility 2 (3) 7 (10) Asymptomatic 19 (32) 4 (6) Abdominal mass 5 (8) 2 (3) Deep vein thrombosis 2 (3) 0 Sixty-nine women (96%) underwent laparoscopic treatment of endometrioma. Two of the remaining women (bilateral endometriomas in both cases) underwent an elective total abdominal hysterectomy and bilateral salpingo-oophorectomy. A laparotomy was also performed in one false positive case (Hirschsprung s disease). Of the group of women undergoing 142 Ultrasound in Obstetrics and Gynecology

4 surgery for a presumed dermoid cyst, 40 (67%) were treated laparoscopically. One laparoscopic case was converted to a laparotomy. DISCUSSION We have demonstrated that a subjective assessment of ovarian morphology, based on characteristic ultrasonographic findings, is highly predictive for the diagnosis of dermoids and endometriomas in a population with a low background risk of ovarian malignancy. The subjective evaluation that any experienced sonographer uses when assigning significance to particular ultrasonographic findings, such as size, echogenicity, the presence of papillary projections and blood flow indices within an adnexal mass, has been shown to be an accurate discriminator between benign and malignant adnexal masses 11. Not everyone has the experience to make these decisions. Morphologic scoring systems and statistical models, such as those involving multivariate logistic regression analysis and more recently artificial neural networks, have been developed. They aim to try to mimic the processes of evaluation that occur within the mind of an experienced sonographer in assigning a risk of malignancy when presented with a number of parameters concerning a given patient or lesion 2,3. Considerable overlap exists between the individual sonographic findings that are used to define the malignant and benign features of a mass. This is especially true of benign cystic teratomas and ovarian malignancy. The presence of solid components within benign cystic teratomas means that, in the context of morphologic scoring systems, dermoids will often score as being highly suspicious of malignancy. For example, Sassone et al. 12 assessed the sonographic characteristics of 39 histologically proven dermoids using a morphology scoring system. Thirty-two of the dermoids had a score of 9, representing a potentially malignant mass 10. It is our contention that some lesions can be diagnosed on the basis of subjective impression, negating the use of complex scoring systems or models. A previous study 11 has shown that, based on subjective impression, the majority of adnexal masses are easy to characterize, with agreement between operators of varying experience in 65% of cases. Approximately 10% of cases were difficult to classify by the least experienced operators (in particular tubo-ovarian abscesses and cystadenofibromas), and it is on the classification of these cases that mathematical models should concentrate. It is not only imperative to differentiate benign from malignant masses, but in a population where the background risk of ovarian malignancy is low, the characterization of benign cyst type is also important. Transvaginal ultrasonography, when used alone, can differentiate dermoids and endometriomas from other adnexal pathology with a specificity of 98% and 90%, respectively 3,4. For the diagnosis of endometrioma, Kurjak and Kupesic 13 improved the accuracy by developing a scoring system combining serum CA125 and transvaginal ultrasonography with color Doppler. Others have been unable to repeat these results 6,14. The clarification of cyst type is important because the mainstay of treatment for both endometriomas and dermoids is surgical, as dermoids undergo torsion or rupture in over 10% of cases 15 and endometriomas do not respond well to medical therapy alone 16. The evolution of laparoscopic surgery has increased the importance of the accurate preoperative assessment of patients. Although a number of studies have advocated the use of minimally invasive surgical techniques in the management of suspected ovarian malignancy 17,18, it has a major role in the treatment of benign ovarian pathology. Transvaginal ultrasonography forms the basis of the assessment of women undergoing surgery for a suspected adnexal mass. With good case selection, benign cystic teratomas can be treated laparoscopically 19. If we can be confident in our diagnosis, patients who may present a poor anesthetic risk can be managed conservatively and those with small dermoids managed expectantly. Endometriosis may be suspected clinically, but definitive confirmation of the diagnosis is made by laparoscopy. The use of ultrasound in its diagnosis has so far been limited to the demonstration of features classically associated with endometriotic cysts 2. It may, however, be useful in the prediction of surgical difficulty likely to be encountered. If advanced pelvic disease is suspected, referral to a tertiary center specializing in laparoscopic management of endometriosis is warranted, negating the need for a primary procedure to confirm the diagnosis. In a research setting, if we can accurately predict the presence of an endometrioma using ultrasound alone, we can accurately monitor cyst recurrence non-invasively following different management regimes. This may be important, as second look laparoscopy is not universally advocated and it has been shown that 27.5% of ovarian endometrioma recurrence is asymptomatic 20. Endometriomas and dermoids comprise the largest proportion of persistent benign adnexal masses in young women. We have demonstrated that transvaginal ultrasonography can reliably predict the presence of these cysts in a population with a low background risk of ovarian malignancy, based on the recognition of characteristic morphologic patterns. The implications for surgery are clear. There is no excuse for poor preoperative assessment of women with a suspected adnexal mass. ACKNOWLEDGMENTS We are grateful to Keymed Ltd. (Southend, UK) and to the Aloka Co. Ltd. (Tokyo, Japan) for the use of their ultrasound equipment. REFERENCES 1 Yeun PM, Yu KM, Yip SK, Lau WC, Rogers MS, Chang A. A randomised prospective study of laparoscopy and laparotomy in the management of benign ovarian masses. Am J Obstet Gynecol 1997; 177: Tailor A, Jurkovic D, Bourne TH, Collins WP, Campbell S. Sonographic prediction of malignancy in adnexal masses using multivariate logistic regression analysis. Ultrasound Obstet Gynecol 1998; 10: Timmerman D, Verrelst H, Bourne TH, De Moor B, Collins WP, Vergote I, Vandewalle J. Artificial neural network models for the preoperative discrimination between malignant and benign adnexal masses. Ultrasound Obstet Gynecol 1999; 13: Ultrasound in Obstetrics and Gynecology 143

5 4 Kupfer MC, Schwimer SR, Lebovic T. Transvaginal sonographic appearance of endometrioma: spectrum of findings. J Ultrasound Med 1992; 11: Mais V, Guerriero S, Ajossa S, Angiolucci M, Paoletti AM, Melis GB. The efficiency of transvaginal ultrasonography in the diagnosis of endometrioma. Fertil Steril 1993; 60: Mais V, Guerriero S, Ajossa S, Angiolucci M, Paoletti AM, Melis GB. Transvaginal ultrasonography in the diagnosis of cystic teratoma. Obstet Gynecol 1995; 85: Koonings PP, Campbell K, Mishell D, Grimes D. Relative frequency of ovarian neoplasms: a 10 year review. Obstet Gynecol 1989; 74: Alcazar JL, Laparte C, Jurado M, Lopez-Garcia G. The role of transvaginal ultrasonography combined with color velocity imaging and pulsed Doppler in the diagnosis of endometrioma. Fertil Steril 1997; 67: Hertzberg BS, Kliewer MA. Sonography of benign cystic teratoma of the ovary: pitfalls in diagnosis. Am J Roentgenol 1996; 167: Cohen L, Sabbagha R. Echo patterns of benign cystic teratomas by transvaginal ultrasound. Ultrasound Obstet Gynecol 1993; 3: Timmerman D, Schwarzler P, Collins WP, Claerhout F, Coenen M, Amant F, Vergote I, Bourne TH. Subjective assessment of adnexal masses with the use of ultrasonography: an analysis of interobserver variability and experience. Ultrasound Obstet Gynecol 1999; 13: Sassone AM, Timor-Tritsch IE, Artner A, Westhoff C, Warren WB. Transvaginal sonographic characterization of ovarian disease: evaluation of a new scoring system to predict ovarian malignancy. Obstet Gynecol 1991; 78: Kurjak A, Kupesic S. Scoring system for prediction of ovarian endometriosis based on transvaginal color and pulsed Doppler sonography. Fertil Steril 1994; 62: Guerriero S, Mais V, Ajossa S, Angiolucci M, Paoletti AM, Melis GB. Transvaginal ultrasonography combined with CA-125 plasma levels in the diagnosis of endometrioma. Fertil Steril 1996; 65: Ahyan A, Aksu T, Develioglu O, Tuncer ZS, Ayhan A. Complications and bilaterality of mature ovarian teratomas (clinicopathological evaluation of 286 cases). Aust NZ Obstet Gynecol 1991; 31: Donnez J, Nisolle M, Gillerot S, Anaf V, Clercx-Braun F. Ovarian endometrial cysts: the role of GnRH agonist and/or drainage. Fertil Steril 1994; 64: Canis M, Pouly JL, Wattiez A, Mage G, Manhes H, Bruhat MA. Laparoscopic management of adnexal masses suspicious at ultrasound. Obstet Gynecol 1997; 89: Childers JM, Nasseri A, Surwit EA. Laparoscopic management of suspicious adnexal masses. Am J Obstet Gynecol 1996; 175: Shalev E, Bustan M, Romano S, Goldberg Y, Ben-Shlomo I. Laparoscopic resection of ovarian benign cystic teratomas: experience with 84 cases. Hum Reprod 1998; 13: Busacca M, Marana R, Caruana P, Candiani M, Muzii L, Calia C, Bianchi S. Recurrence of ovarian endometrioma after laparoscopic excision. Am J Obstet Gynecol 1999; 180: Ultrasound in Obstetrics and Gynecology

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