Smita Jain, M.B., M.S.* and Maureen E. Dalton, F.R.C.O.G. Sunderland Royal Hospital, Sunderland, Tyne and Wear, United Kingdom

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1 ENDOMETRIOSIS FERTILITY AND STERILITY VOL. 72, NO. 5, NOVEMBER 1999 Copyright 1999 American Society for Reproductive Medicine Published by Elsevier Science Inc. Printed on acid-free paper in U.S.A. Chocolate cysts from ovarian follicles Smita Jain, M.B., M.S.* and Maureen E. Dalton, F.R.C.O.G. Sunderland Royal Hospital, Sunderland, Tyne and Wear, United Kingdom Objective: To study the development of chocolate cysts by serial transvaginal ultrasonographic tracking of ovarian follicles. Design: Retrospective study. Setting: Department of Obstetrics and Gynaecology, Sunderland Royal Hospital, Sunderland, United Kingdom. Patient(s): We reviewed case notes of all patients who underwent laparoscopy for diathermy to endometriosis/ovarian diathermy/aspiration of ovarian cysts from 1989 to Twelve women with histories of infertility and proven chocolate cysts with documented ultrasonographic findings were included in the study. Intervention(s): Serial ultrasonographic tracking of ovarian follicles in the cycle leading to the development of the chocolate cysts, followed by ultrasonographic tracking of cysts for 3 months and laparoscopy. Main Outcome Measure(s): Development and formation of chocolate cysts. Result(s): The diagnosis of chocolate cysts was confirmed laparoscopically in all patients and histopathologically in four. Ultrasound confirmed that they had all developed from follicles. Conclusion(s): Chocolate cysts can develop from ovarian follicles. (Fertil Steril 1999;72: by American Society for Reproductive Medicine.) Key Words: Chocolate cyst, transvaginal ultrasonography, laparoscopy, endometriosis, endometrioma Received January 25, 1999; revised and accepted June 1, Reprint requests: Maureen E. Dalton, F.R.C.O.G., Department of Obstetrics & Gynaecology, Sunderland Royal Hospital, Sunderland SR4 7TP, United Kingdom (FAX: ; m.dalton@bt.internet.com). * Present address: Department of Obstetrics and Gynaecology, Royal Devon and Exeter Hospitals (Heavitree), Exeter, United Kingdom. Department of Obstetrics and Gynaecology, Sunderland Royal Hospital /99/$20.00 PII S (99) The term chocolate cyst was used by Sampson in 1921 to describe an endometrial cyst of the ovary (1) and chocolate cyst and endometrial cyst are used interchangeably. The most typical lesions in ovarian endometriosis are endometrial cysts (endometriomas). The presence of a chocolate cyst indicates a more advanced stage of endometriosis (2). The revised American Society for Reproductive Medicine classification of endometriosis is widely accepted (3). It takes into account the extent of disease and the amount and severity of adhesions. In this system, endometriosis is classified as stage 1 (minimal), stage 2 (mild), stage 3 (moderate), or stage 4 (severe). Ovarian endometriotic cysts may be confirmed histologically or by determining whether all of the following criteria are met: cyst diameter of 12 cm, adhesion to the pelvic side wall and broad ligament, endometriosis on the surface of the ovary, and tarry, thick, chocolate-colored fluid content. The diagnosis of ovarian endometrial cyst is usually based on visualization during laparoscopy, which has a sensitivity of 97%, a specificity of 95%, and an overall accuracy of 96%, and also by aspiration of the chocolate-colored fluid (4), with histologic confirmation. The presence of chocolate-colored fluid may be misleading because this fluid can also be found in other cysts, such as lutein cysts and even some neoplastic cysts (5). The aim of this study was to show, by serial transvaginal ultrasonographic tracking of ovarian follicles, that a chocolate cyst can develop from an ovarian follicle. MATERIALS AND METHODS This retrospective study was done at the Sunderland Royal Hospital, a district general hospital in northeast England that serves a population of approximately 350,000. We reviewed one consultant s cases from the period Because our study was a retrospective review of case notes and did not involve human experimentation in any form, our institution did not require ethics board approval. The data recorded included demographics, ultrasonographic documentation of ovarian fol- 852

2 FIGURE 1 Ovarian follicle. licle development (follicle tracking), and laparoscopic and histologic findings. This study included 12 women who were ultrasonographically monitored in the fertility clinic. During cycles of follicle tracking, the development of chocolate cysts with typical fluid in-filling was observed, and these chocolate cysts were further tracked for up to 3 months before laparoscopy (Figs 1 to 3). Patients were between 26 and 36 years of age, and the duration of infertility was between 1 and 12 years. Findings of basic investigations for infertility were normal. Follicular development was monitored by transvaginal sonography (Toshiba Sonolayer SSH 140A; Toshiba, Japan), with 3.5- and 7-MHz probes. Ultrasonography was performed from day 9 of the menstrual cycle initially, on alternate days, until the mean follicular diameter exceeded 14 mm, and daily thereafter. Follicles were measured in three planes and the average diameter was determined. The follicles were tracked and characteristic in-filling was noted; then scanning was performed at weekly intervals (Fig. 4). The sonographic criteria for the diagnosis of endometrioma were a cystic structure with low, homogeneous echogenicity and a thick cystic wall with regular margins. One important criterion for diagnosis of chocolate cysts by ultrasonography was the persistence of a cyst for at least two consecutive cycles. This permitted us to distinguish a corpus luteum cyst from an endometrioma. Corpus luteum cysts, whose sonographic patterns are usually different from those of endometriomas, should regress spontaneously at the end of the menstrual cycle. A corpus luteum cyst looks somewhat like an octopus, in that the center is occupied by a blood clot and some highly echogenic branches ramify into the cystic fluid (6). We also recorded grading of the endometrium during the menstrual cycle when the in-filling was observed based on the thickness and reflectivity. For endometrial grading, the gray-scale appearance of endometrial texture was compared with that of myometrial texture. Four patterns of endometrial response can be distinguished (7). After the 3 months of scans, laparoscopy was performed under general anesthesia. The diagnosis of chocolate cysts was confirmed laparoscopically in all patients and histopathologically in four. Endometriosis was staged according to the revised American Fertility Society classification. In all 12 patients, chocolate cysts were diathermized or drained, and treatment with danazol or goserelin was begun immediately after laparoscopy and continued for 6 months. Endometrial spots seen elsewhere were diathermized and adhesiolysis was performed if indicated. FERTILITY & STERILITY 853

FIGURE 2 Ovarian follicle increased in size. Patients were evaluated at 6 weeks and were further followed up depending on symptoms and fertility treatment.

3 FIGURE 2 Ovarian follicle increased in size. Patients were evaluated at 6 weeks and were further followed up depending on symptoms and fertility treatment. RESULTS The mean age of the 12 patients was 30.4 years, the mean age at menarche was 13.1 years, and the average duration of menstrual cycles was 28.6 days. All patients presented with infertility and dysmenorrhea either before menstruation or on day 1, 2, or 3 of the cycle. There was no significant history in any of these patients. Ten (83%) of 12 patients had moderate endometriosis. Two (17%) had severe endometriosis of one or both ovaries involving other pelvic structures as well. Four (33.33%) had chocolate cysts in the right ovary, 5 (41.66%) had chocolate cysts in the left ovary, and 3 (25%) had bilateral cysts. In all 12 patients, the ovarian follicles developed into chocolate cysts, the average diameter of which was 37 mm (range, mm). Seven of 12 patients were treated with clomiphene or cyclofenil; the rest did not receive any medication. The cysts grew at different rates on the different days of the cycle. Follicles started to fill in between 11 and 18 days. After cysts reached a particular size, growth plateaued. Preovulatory endometrium (grade B) was noted at the time of follicle filling in 10 cycles and early luteal phase endometrium (grade A) was noted in 2 cycles (Table 1). Of the 12 patients who had laparoscopic ovarian diathermy or aspiration of ovarian cysts, 4 became pregnant and 8 did not. Of those 8 patients, 4 were not receiving active treatment and 4 continued receiving treatment and were followed up regularly. DISCUSSION Since the first description of chocolate cysts by Sampson in 1921 (1), endometriosis has remained a puzzling disease, one of unknown histogenesis and etiology. The ovary is most commonly affected by endometriosis and is involved in approximately 50% of patients with endometriosis. Ovaries irregular surfaces favor development of endometriosis. The local steroid hormone environment may be a facilitating factor. Ovarian endometriomas account for 35% of benign ovarian cysts (8). Hughesdon (9) performed serial sections of endometriotic ovaries and found that in 90% of cases, the endometriotic wall consisted of ovarian cortex, demonstrated by the presence of primordial follicles. This observation lent support to this hypothesis that this type of lesion originates at the surface, through implantation or metaplasia, with subsequent invagination of the ovarian cortex. The pseudocyst is likely 854 Jain and Dalton Chocolate cysts Vol. 72, No. 5, November 1999

(10) by ovarioscopy and biopsy. In 1990, Martin and Berry (11) showed that not all ovarian chocolate cysts have histologic evidence of endometriosis.

4 FIGURE 3 Ovarian follicle filled in (chocolate cyst). to be formed by hematoma that causes invagination of ovarian cortex, which is subsequently colonized by endometrial surface with or without stroma. This was confirmed by Brosens et al. (10) by ovarioscopy and biopsy. In 1990, Martin and Berry (11) showed that not all ovarian chocolate cysts have histologic evidence of endometriosis. Corpus luteum or corpus albicans was present in 12% of 41 chocolate cysts diagnosed as endometriomas at the time of laparoscopy. FIGURE 4 Ultrasonographic tracking of ovarian follicle of patient 1. *, follicle filled in. TABLE 1 Ultrasonographic findings. Patient no. Size of follicle on day 1 (mm)* Day follicle was filled in Day follicle size attained plateau Grade of endometrium at time of filling A B/C B B B B A B B B B B * Mean SD, mm. Mean SD, day Mean SD, day Jain. Chocolate cysts from. Fertil Steril FERTILITY & STERILITY 855

5 On the basis of clinical appearance and histology, endometriomas have been classified as primary (type I) and secondary (type II) (12). Ovarian endometriosis is known to be associated with symptoms of infertility and pelvic pain. Differentiation of ovarian endometriotic cysts from cystic corpora lutea is clinically important because cystectomies for corpora lutea should be avoided in women with infertility, given the risk of postoperative adhesion formation. Although we ascertained in our study that chocolate cysts can originate from the ovarian follicle, the source of the fluid in the cysts remains unclear and many hypotheses have been suggested. Nieminen (13) suggested that free superficial implants undergo advanced secretory changes at the end of the menstrual cycle and show vascular necrosis and shedding at the time of menstruation. The small mucosal implants and congested vessels near the hilus of the ovary have been shown to be responsible for the bleeding in chocolate cysts. Our study confirms the findings by Donnez et al. (14) that endometrial shedding was not responsible for the bleeding in cysts. They demonstrated the presence of chocolate-colored fluid 3 months after drainage of endometrioma and administration of GnRH agonist therapy. The diagnosis of chocolate cyst was confirmed laparoscopically in all patients and histopathologically in 4 of the 12 patients. Chocolate cysts may play a small role in the development of endometriosis and should be considered in the evaluation of infertile couples. In conclusion, we found that ovarian follicles can grow and develop into chocolate cysts and that this occurs more often than previously thought in women with endometriosis. Our observational study was retrospective and involved a small number of patients. A larger prospective cohort study might permit the true incidence of this condition to be ascertained. Acknowledgments. The authors thank S. A. Bober, B.Sc., M.B.B.S., F.R.C.O.G. Department of Obstetrics and Gynaecology, West Cumberland Hospital, Whitehaven, United Kingdom, for his expert comments during the preparation of this article; Ms. Maureen Raine and staff of the Department of Medical Records, Sunderland Royal Hospital; and Mrs. Wendy Scoon and Mrs. Val Williams for manuscript preparation. They are also thankful to Mrs. D. L. Richardson, Mr. Graham Slocombe, and the staff of Fotografix department of Royal Devon and Exeter Hospitals, for their assistance in preparing illustrations. References 1. Sampson JA. Perforating hemorraghic (chocolate) cysts of the ovary. Arch Surg 1921;3: Nakahara K, Saito H, Saito T, Ito M, Ohta N, Takahashi T, et al. Ovarian fecundity in patients with endometriosis can be estimated by the incidence of apoptotic bodies. Fertil Steril 1998;69: American Society for Reproductive Medicine. Revised American Society for Reproductive Medicine classification of endometriosis: Fertil Steril 1997;67: Vercellini P, Vendola N, Bocciolone L, Rognoni MT, Carinelli SG, Candiani GB. Reliability of the visual diagnosis of ovarian endometriosis. Fertil Steril 1990;56: Brosens I, Puttemans P, Deprest J. Appearances of endometriosis. Baillieres Clin Obstet Gynaecol 1993;7: Rottem S, Levit N, Thaler I, Yoffe N, Bronshtein M, Manor D, et al. Classification of ovarian lesions by high-frequency transvaginal sonography. J Clin Ultrasound 1990;18: Smith B, Porter R, Ahuja K, Craft I. Ultrasonic assessment of endometrial changes in stimulated cycles in an in vitro fertilization and embryo transfer program. J In Vitro Fert Embryo Transf 1984;1: Prevalence and anatomical distribution of endometriosis in women with selected gynaecological conditions: results from a multicentric Italian study. Gruppo italiano per lo studio dell endometriosi. Hum Reprod 1994;9: Hughesdon PE. The structure of endometrial cysts of the ovary. J Obstet Gynaecol Br Emp 1957;44: Brosens IA, Puttemans P, Deprest J. The endoscopic localization of endometrial implants in the ovarian chocolate cyst. Fertil Steril 1994; 61: Martin DC, Berry JD. Histology of chocolate cysts. Gynaecol Surg 1990;6: Nezhat F, Nezhat C, Allan CJ, Metzger D, Sears D. Clinical and histologic classification of endometriomas. J Reprod Med 1992;37: Nieminen U. Studies on the vascular pattern of ectopic endometrium with special reference to cyclic changes. Acta Obstet Gynecol Scand 1962;41: Donnez J, Nisolle MM, Cananas RF, et al. Endometriosis: rationale for surgery. In: Brosens I, Donnez J, eds. The current status of endometriosis research and management. Parthenon, 1993: Jain and Dalton Chocolate cysts Vol. 72, No. 5, November 1999

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