Ovarian Carcinoma in Patients with Endometriosis: MR Imaging Findings

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1 Yumiko Oishi Tanaka 1 Takeshi Yoshizako 1,2 Masato Nishida 3 Masayuki Yamaguchi 1 Kazuro Sugimura 2 Yuji Itai 1 Received June 4, 1999; accepted after revision April 20, Department of Radiology, Institute of Clinical Medicine, University of Tsukuba, Tennodai, Tsukuba, Ibaraki , Japan. Address correspondence to Y. O. Tanaka. 2 Department of Radiology, Shimane Medical University, 89-1 Enya, Izumo, Shimane , Japan. 3 Department of Obstetrics and Gynecology, Institute of Clinical Medicine, University of Tsukuba, Tsukuba, Ibaraki , Japan. AJR 2000;175: X/00/ American Roentgen Ray Society Ovarian Carcinoma in Patients with Endometriosis: MR Imaging Findings OBJECTIVE. Various types of malignancy can develop in patients with endometriosis. Enhancing mural nodules have been reported as an imaging characteristic of malignant transformations. We evaluated contrast-enhanced MR imaging to determine the optimum sequence to reveal mural nodules and other characteristics of malignant transformations. MATERIALS AND METHODS. We examined 10 patients with pathologically proven ovarian adenocarcinoma in endometriosis and 10 patients (the control group) with ovarian endometrioma suggestive of malignant transformation on the basis of sonographic findings. We analyzed the size and nature of the endometriomas in each patient. We compared four types of contrast-enhanced MR imaging to determine which sequence best revealed mural nodules. RESULTS. In the malignant and control groups, 80% of the cysts with findings suggestive of malignant transformation showed unilateral disease or larger endometrial cysts on the suggestive side than on the contralateral side. High signal intensity on T1-weighted images and low signal intensity on T2-weighted images relative to the myometrium were observed only in two of 10 malignant endometrial cysts and in all control cysts. All malignant endometriomas had small mural nodules with low signal intensity on T1-weighted contrast-enhanced images. Only three benign endometriomas had mural nodules and none of them enhanced. The enhancement of mural nodules was easily seen on dynamic subtraction imaging. CONCLUSION. On the basis of our findings, endometrial cysts with malignant transformation rarely show low signal intensity on T2-weighted images and usually have enhancing mural nodules. Because the enhancement of mural nodules is often difficult to evaluate on conventional T1-weighted images, dynamic subtraction imaging can be valuable. E ndometriosis is a common disease that affects women of reproductive age [1]. Although the disease is recognized as benign, endometriosis is occasionally accompanied by malignant ovarian tumors, especially endometrioid and clear cell adenocarcinomas [2 9]. However, to the best of our knowledge, the imaging features of malignant ovarian tumors have not been published in the English literature [10, 11]. We examined 10 patients with ovarian cancer in endometriosis. We describe the MR imaging features of ovarian cancer in endometriosis and emphasize the use of dynamic subtraction MR imaging to diagnose this entity. Materials and Methods Ten patients with surgically and pathologically proven primary ovarian adenocarcinoma in endometriomas were examined from 1992 to All patients had cancer that satisfied the criteria for malignant change in endometriosis according to Sampson [2]: endometriosis and carcinoma coexisting in the same ovary; carcinoma in the region of endometriosis that is not metastatic; and a transitional lesion between the carcinoma focus and the endometriosis lesion. Transitional lesions are ectopic endometrium with mild to severe atypia consecutive between the endometrium without atypia and adenocarcinoma. Our patients were from 32 to 51 years old (mean age, 43 years) at the time of the diagnosis. Four patients were asymptomatic, two had lower abdominal pain, two had cystitis, one had irregular menstruation, and one had dysuria. Cancer antigen 125 antigen levels were elevated in eight of nine patients, and cancer antigen 19-9 tumor markers were elevated in five of nine patients. Three patients had a history of hormone therapy for endometriosis from 1 to 3 years before MR imaging. Radical surgery for ovarian cancer in each institute was performed within 3 weeks of MR imaging. Endometriosis was proven in all patients. Pathologic diagnosis was confirmed as clear cell adenocarcinoma (n = 6), endometrioid adenocarcinoma (n = 2), and mixed adenocarcinoma (n = 2). All carcinoma was diagnosed as ovarian carcinoma developing from endometriosis, according to the criteria of Sampson [2]. Pathologic stage of ovarian cancer was AJR:175, November

2 Tanaka et al. stage Ia in two patients, Ic in three, IIa in one, IIc in two, and IIIc in two. MR imaging was performed with a Gyroscan 1.5-T superconducting magnet (Philips, Best, The Netherlands) in five patients, a Signa 1.5-T superconducting magnet (General Electric Medical Systems, Milwaukee, WI) in three patients, and a 1.0-T superconducting magnet (Magnex 100; Shimadzu, Kyoto, Japan) in two patients. Axial T1-weighted spin-echo (TR range/ TE range, /11 15) and axial T2-weighted spin-echo ( /80 90) or fast spin-echo ( /88 110) images were obtained in all patients. Contrast-enhanced T1-weighted axial images with 5 mmol of meglumine gadopentetate (Magnevist; Nihon-Schering, Osaka, Japan) were also obtained in all patients. Contrast-enhanced T1-weighted MR imaging was performed with a fat-saturation technique in three patients and a dynamic technique in four. The slice thickness was 5 10 mm, intersection gap was mm, and data were collected with matrices of Field-of-view measurements were cm, and the number of excitations was two for T1- and T2-weighted images. T1-weighted gradientecho images (11 15/ ; flip angle, ) were obtained every sec after the administration of contrast material on the Gyroscan scanner, and a fastfield-echo technique was used. The slice thickness was 10 mm, matrix was , field of view was 28 cm, and number of excitations was six. Dynamic subtraction contrast-enhanced images were synthesized in three of four patients after the examination. MR images were interpreted by two radiologists who reached consensus agreement after discussing the TABLE 1 findings. In each patient, we analyzed the volume of each adnexal mass; nature of the mass, including the presence of loculations; signal intensity; volume ratio of the endometrial cysts with ovarian cancer compared with the contralateral benign endometrial cysts; size of the mural nodules in maximum diameter; and nature of the mural nodules, including shape, signal intensity, and contrast enhancement. Each endometrioma was considered an oval globe, and its volume was roughly calculated using the following equation: V = 4 / 3 π a 2 c Where V is volume, a is transverse diameter divided by two, and c is height divided by two. We noticed that endometriomas with malignant transformation were larger than contralateral benign endometriomas. We then needed some indexes, which would have shown the asymmetry of the ovarian endometriomas. Therefore, volume ratio is not a common measure, although we used this index. The shape of mural nodules was classified as nodular when the surface of the nodule was smooth and as papillary when the surface was irregular. Signal intensity of each nodule was compared with that of myometrium on T1- weighted images and compared with that of outer myometrium on T2-weighted images. We determined the presence or absence of enhancement of mural nodules by visual inspection. During the same period, we examined 10 patients (age range, years; mean age, 38 years) with endometriosis and mural nodulelike structures on sonography. Although pathologic diagnosis for endometrioma was confirmed in only five patients, none of the remaining endometriomas grew larger during MR Imaging Findings of Patients in Study Group and Control Group Finding No. of Patients in Study Group Control Group or after the study (follow-up examinations, 3 34 months). These patients were our control group. Patients underwent MR imaging on one of two 1.5-T superconducting units (Signa [n = 1] or Gyroscan [n = 9]) with the same technique as that for the malignant cohort. For three patients with mural nodulelike structures, contrast enhancement was evaluated on dynamic contrast-enhanced and dynamic subtraction images in two patients and on fat-saturated T1- weighted images in one patient. We also analyzed which sequence was best for evaluating contrast enhancement: T1-weighted images (n = 12); fat-saturated T1-weighted images (n = 4); dynamic contrast-enhanced images (n = 6); or dynamic subtraction contrast-enhanced images (n = 5). In one patient, two MR examinations were available for review: dynamic contrast-enhanced T1- weighted images were obtained 2 weeks before surgery and conventional T1-weighted images were obtained 18 months before surgery. Results A summary of MR imaging features of benign and malignant endometriomas is shown in Table 1. For all patients with malignant endometriomas, we found one or two cystic masses in the pelvis. Although some of these lesions could be extraovarian endometriomas, a normal ovary was not visible on the involved side; therefore, the lesions were presumed to be ovarian endometriomas. This assumption could not be proven on imaging. Adnexal masses with Finding No. of Patients in Volume ratio suggestive of malignant/contralateral Maximum diameter of mural nodules (cm) >1.0 and >3.0 and > > Unilateral 4 6 Shape of mural nodules Maximum diameter of cyst suggestive of malignancy Nodular Papillary 4 0 >5.0 and Angle of attachment of mural nodules > Acute 9 2 Area with low signal intensity on T2-weighted images and high Obtuse 1 1 signal intensity on T1-weighted images Obvious 2 10 Signal intensity of mural nodules Equivocal 2 0 On T1-weighted images None 6 0 Low 10 0 Locularity Intermediate 0 1 Unilocular 3 3 High 0 2 Multilocular 7 7 On T2-weighted images Low 2 3 Intermediate 2 0 High 6 0 Study Group Control Group 1424 AJR:175, November 2000

3 MR Imaging of Ovarian Carcinoma in Endometriosis characteristics of endometrial cysts, including a thick capsule or adhesion to adjacent structures, were observed bilaterally in six of 10 patients and unilaterally in four. In six patients with bilateral endometriomas, the ovarian cancer developed unilaterally in one of the endometrial cysts, as previously reported by Sampson [2]. Conversely, we found cystic masses with typical MR imaging features for bilateral ovarian endometrioma in four patients in the control group and for unilateral ovarian endometrioma in six. The mean diameter of the endometriomas with malignant transformation and in the control group were 9.4 cm and 5.0 cm, respectively. The sizes of unilateral endometrial cysts with associated cancers were larger than those of contralateral endometrial cysts in five patients and smaller in one patient of six with bilateral lesions (Figs. 1 and 2). In the control group, the size of endometrial cysts with mural Fig year-old woman with clear cell adenocarcinoma that developed from endometrial cyst of right ovary. Patient had history of administration of danazol to control endometriosis. A, Axial spin-echo T1-weighted MR image (TR/TE, 500/15) shows multilocular cystic mass (M) that includes hyperintense fluid behind uterus (U). Bilateral cysts and uterus have adhered to one another as shown by absence of fat between them. B, Axial fast spin-echo T2-weighted MR image (4000/88) shows extensive shading on left cyst (L). Note signal loss on right cyst is limited to small area. C, Axial spin-echo T1-weighted MR image (500/15) slightly cranial to A and B reveals small hypointense mural nodule (arrow) on wall of right cyst. Left endometrial cyst cannot be seen at this level. Most of mural nodule shows higher signal intensity than outer myometrium of uterus as seen on B. D, Contrast-enhanced axial spinecho T1-weighted MR image (500/ 15) shows weakly enhanced mural nodule. It is difficult to evaluate contrast enhancement because of hyperintense fluid surrounding mural nodule. nodules on sonography was at least five times larger than that of contralateral endometrial cysts in two patients, the size was larger but less than five times the size in one patient, and the size was smaller in one of four patients with bilateral disease. On T1-weighted images, 29 of 30 endometriomas in both groups of patients showed significantly higher signal intensity than myometrium; the remaining endometrioma with malignant transformation showed slightly higher signal intensity compared with that of the myometrium. For both the ovarian cancer and control groups, the endometrial cysts were multilocular in seven patients and unilocular in three patients. High signal intensity on T1- weighted images and low signal intensity on T2-weighted images relative to the myometrium were observed in only two of the 10 endometrial cysts complicated with ovarian cancer. Conversely, all six contralateral cysts C A without ovarian cancer and all 14 cysts in the control group showed high signal intensity on T1-weighted images and low signal intensity on T2-weighted images (Fig. 2). One or several mural nodules were observed in all the endometrial cysts complicated with cancer (Figs. 1 3). None of the benign contralateral cysts had mural nodules (Figs. 1 and 2) in the malignant group. In the control group, only three of 10 endometriomas had nonenhancing mural nodules (Fig. 4). The size of the mural nodules in the malignant cysts ranged from 2.0 to 6.5 cm; the mural nodules showed low signal intensity on T1-weighted images and various signal intensity on T2-weighted images compared with that of myometrium. The shapes of the mural nodules were nodular in six patients and papillary in four patients. The nodules protruded from the cyst wall with an acute angle in nine patients and with an obtuse angle in one. Conversely, the B D AJR:175, November

4 Tanaka et al. A E C Fig year-old woman with clear cell adenocarcinoma that developed in endometrial cyst of left ovary. A, Axial spin-echo T1-weighted MR image (TR/TE, 442/14) reveals large multilocular hyperintense cystic mass with mural nodule (arrow) behind uterus. Note smaller right ovarian endometrial cyst (R) is also seen between uterus and larger endometrial cyst. B, Axial fast spin-echo T2-weighted MR image (1836/110) shows signal loss of smaller endometrial cyst (R); however, larger cyst remains hyperintense. Mural nodule shows slight hyperintensity compared with signal of outer myometrium of uterus (U). C, Unenhanced MR image (fast gradient echo; 12/5.1; flip angle, 40 ) of dynamic sequence shows mural nodule on anterior endometrial cyst wall. D, Axial dynamic contrast-enhanced MR image (fast gradient echo; 12/5.1; flip angle, 40 ) obtained 92 sec after administration of contrast material shows enhancement of uterus; however, enhancement of mural nodule is harder to recognize (arrow). E, Unenhanced dynamic subtraction MR image synthesized from C reveals no abnormal pelvic structures or masses with mural nodules. F, Axial dynamic subtraction MR image synthesized from D shows enhancement of root of mural nodule (arrow). B D F 1426 AJR:175, November 2000

5 Fig year-old woman with clear cell adenocarcinoma in endometrial cyst of right ovary. A, Sagittal spin-echo T1-weighted MR image (TR/TE, 500/15) obtained before diagnosis of ovarian cancer reveals unilocular hyperintense cystic mass with mural nodule (arrow). Note smaller endometrial cyst in left ovary on other slice level. B, Contrast-enhanced sagittal spinecho T1-weighted MR image (500/ 15) reveals slight enhancement of mural nodule (arrow). We could not conclude whether the nodule was benign or malignant. C, Sagittal spin-echo T1-weighted MR image (408/15) obtained 18 months after A and B reveals enlarged tumor, mural nodule, and another mural nodule (arrow) visible on anterior wall of endometrial cyst, despite hormone therapy for endometriosis. D, Sagittal fast spin-echo T2- weighted MR image (2076/130) does not show signal loss of endometrial cyst. Mural nodules show lower intensity compared with signal of myometrium. E, Sagittal unenhanced MR image (fast gradient echo; 11/5.6; flip angle, 25 ) of dynamic sequenceshows two hypointense mural nodules on endometrial cyst wall. F, Sagittal dynamic contrast-enhanced MR image (fast gradient echo; 11/5.6; flip angle, 25 ) obtained 99 sec after administration of contrast material shows enhancement of mural nodule on anterior wall of endometrioma. Enhancement of mural nodule on superior wall is harder to recognize. MR Imaging of Ovarian Carcinoma in Endometriosis A C E B D F mural nodularity in the control group ranged from 0.6 to 1.5 cm in size; it showed intermediate (n = 1) and high (n = 2) signal intensity on T1-weighted images and showed low signal intensity (n = 3) on T2-weighted images, compared with that of the myometrium. The shape of the mural nodules was nodular and they protruded from the cyst wall with an acute angle in two patients and an obtuse angle in one patient. The evaluation of contrast enhancement of the mural nodules in the malignant (n = 10) and control (n = 3) groups was often difficult because the signal intensity of the fluid surrounding the mural nodules was similar to that of the mural nodules themselves after the administration of contrast material (Figs. 1 4). Evaluation of contrast enhancement was easy on one of 12 T1-weighted images, on none of AJR:175, November

6 Tanaka et al. four fat-saturated T1-weighted images, on one of six dynamic images, and on five of five dynamic subtraction images (Fig. 5). Discussion Endometriosis is defined as the presence of endometrial tissue outside the uterus, and it can cause extensive adhesions in the pelvis. It affects approximately 7% of women of reproductive age in the United States, and these patients may have abdominal pain or infertility as A D Fig year-old woman with ovarian endometrioma and mural nodule on sonography. A, Sagittal spin-echo T1-weighted MR image (TR/TE, 442/14) reveals multilocular hyperintense mass with slightly more hyperintense area (arrow) on posteroinferior wall. This area corresponds to mural nodule on sonography (not shown). B, Sagittal fast spin-echo T2-weighted MR image (1836/110) shows hyperintense mass with hypointense mural nodule (arrow). C, Sagittal unenhanced MR image (fast gradient echo; 12/5.1; flip angle, 40 ) of dynamic sequence shows high signal intenisty similar to that in A. D, Sagittal dynamic contrast-enhanced MR image (fast gradient echo; 12/5.1; flip angle, 40 ) obtained 117 sec after administration of contrast material does not reveal enhancement of mural nodule (arrowhead). E, Unenhanced dynamic subtraction MR image synthesized from C shows no abnormal pelvic structures or masses with mural nodules. F, Sagittal dynamic subtraction MR image synthesized from D confirms nonenhancement of mural nodule (arrow). a result. The disease is considered benign; however, since Sampson [2] first reported some patients with malignant transformation in endometriosis, pathologists and gynecologic oncologists are aware of a malignant entity. Why endometriosis undergoes malignant transformation remains unknown; however, some investigators have postulated that estrogen may have a role in the development of malignancy [4, 6]. Also implicated in the development of premalignant transformation of endometriosis is estrogenic stimulation, B E such as atypical adenomatous hyperplasia [4]. In patients with endometriosis who develop ovarian cancer, endometrioid adenocarcinoma is the most commonly reported malignant tumor after clear cell adenocarcinoma, when the primary site is the ovary [4, 12]. Extragonadal lesions are reported to be mostly endometrioid tumors and sarcomas [4]. This disease is seen in women who are years younger than those who develop endometrial or ovarian cancer [4]. The incidence of malignancy in ovarian endometriosis is % [4, 5, 13]. F C 1428 AJR:175, November 2000

7 MR Imaging of Ovarian Carcinoma in Endometriosis Fig. 5. Bar chart shows difficulty in evaluation of contrast enhancement of mural nodules with various imaging sequences. We can easily evaluate contrast enhancement of mural nodules on five dynamic subtraction images. Conversely, we can evaluate enhancement in only one of 12 conventional T1-weighted images. Dynamic subtraction imaging is best for evaluating contrast enhancement of mural nodules in endometrial cysts. Conversely, the incidence of endometriosis in patients with ovarian cancer varies from 4.2% to 14.5% [9]. The highest incidence was observed in Japan, which has the lowest incidence of lifetime risk for developing ovarian cancer. This could be an explanation for the incidence of clear cell adenocarcinoma being relatively high in Japan because clear cell adenocarcinoma has the closest relationship to benign pelvic endometriosis [4, 5]. We found two case reports that describe the imaging findings of malignant transformation in extraovarian endometriosis [10, 11]; however, cases of ovarian cancer in endometriosis have not been published in English literature. We found only two Japanese case reports describing ovarian cancer in endometriosis [14, 15]. According to the literature, the presence of mural nodules on the wall of endometrial cysts, which are enhanced by meglumine gadopentetate, is considered key in diagnosing the malignant transformation of endometriosis. However, it is difficult to evaluate the contrast enhancement of mural nodules because endometrial cysts have high signal intensity on T1- weighted images caused by the presence of deoxyhemoglobin or methemoglobin from old hemorrhage [16], and the mural nodules are often very small [14, 15]. Therefore, our goal was to describe the MR imaging features of the malignant transformation of endometriosis and to find the most useful method to evaluate the contrast enhancement of the mural nodules surrounded by hyperintense fluid on T1-weighted images. Endometrial cysts have been reported to be hyperintense on T1-weighted images with multiplicity, a thick fibrous capsule, or adhesions to surrounding organs [16, 17]. On T2- weighted images, the endometrial cysts have low signal intensity. In our study, all 10 masses with malignant transformation showed hyperintensity on T1-weighted images and had thick walls (maximum thickness, >3 mm). However, only two of 10 endometrial cysts with malignant transformation showed low signal intensity on T2-weighted images compared with six contralateral benign cysts. Togashi et al. [17] reported that low signal intensity on T2-weighted images was noted in 55 (64%) of 86 benign endometrial cysts. The incidence of low signal intensity on T2-weighted images in our malignant transformation group was lower (20%) than that in their report. Additionally, all 10 masses in the control group had low signal intensity on T2-weighted images. This intensity pattern is believed to be caused by a magnetic susceptibility effect generated by hemosiderin in old hemorrhage, densely concentrated fluid, or fibrosis [16]. Because MR imaging findings of most ovarian carcinomas were reported to be mixed solid and cystic tumors [18], we speculate that adenocarcinomas in endometriosis may produce some fluid. Then once malignant transformation occurs, the fluid can dilute thick hemorrhagic fluid. This process may be the reason why endometrial cysts with malignant transformation seldomly show low signal intensity on T2-weighted images and tend to be large cysts. Although the mean diameter of the endometriomas with malignant transformation was larger than that in the control group, we could not determine the threshold size for malignant transformation of endometrial cysts because there was a lot of overlap between the malignant and control groups. The size of endometriomas with malignant transformation tended to be larger than contralateral benign cysts in the malignant group. However, in eight of 10 control patients, the endometrial cysts suggestive of malignancy were unilateral or larger than contralateral endometrial cysts. Therefore, for diagnosing this entity, the asymmetry of the endometriomas did not seem as important as signal intensity on T2-weighted images. As mentioned before, endometrial cysts tend to be multiloculated; however, three of 10 cysts were unilocular (Fig. 3). They had thick walls and hyperintense fluid on T1- weighted images. Prospective diagnosis of endometriosis was difficult, especially when contralateral cysts did not show typical features of endometriomas. The signal intensity of the mural nodules was low on T1-weighted images in all 10 malignant nodules; however, the signal intensity on T2-weighted images was variable in each nodule and not related to histologic subtype. This finding may be caused by cellularity or the degree of stromal edema rather than histologic subtype. Also, the shape of the mural nodules was not related to histologic subtype. Because the maximum diameter of the mural nodules surrounded by hyperintense fluid was smaller than 3 cm in six of 10 malignant and three control nodules, it was difficult to evaluate whether the nodules enhanced after the administration of meglumine gadopentetate. This difficulty was caused by the enhancement of the uterus and other adjacent structures and the increase in background signal intensity. We used fat-saturated T1-weighted images, dynamic contrast images, and dynamic subtraction images to evaluate the presence or absence of enhancement. Although contrast-enhanced MR imaging was performed with different techniques in each patient, all the radiologists who evaluated the MR images judged that the dynamic subtraction images were the best to visualize the enhancement of mural nodules, followed by the dynamic images and the fat-saturated T1-weighted images. We could not diagnose malignant transformation in one patient (Fig. 3), with MR images obtained 18 months before diagnosis. In that study, only conventional T1-weighted images were obtained after the administration of contrast material, and we could not evaluate positive enhancement of the mural nodule. Eighteen months later, the mass was bigger and another mural nodule appeared. At the time the patient s condition was diagnosed as malignant transformation, peritoneal dissemination had already occurred; she died of carcinoma 3 years after the diagnosis. AJR:175, November

8 Tanaka et al. Sonography, especially transvaginal scanning, is used to identify adnexal masses and may play a role in identifying malignant transformation. However, although endometrial cysts are typically round and homogeneously hypoechoic [19, 20], epithelial ovarian carcinomas typically appear as anechoic thin-walled cysts with echogenic endocystic vegetation [21] on sonography. It may be as difficult to detect tiny echogenic endocystic components. Also, it may be as difficult on sonography as on T1- weighted MR imaging to detect enhanced mural nodules. Furthermore, blood clot or focal fibrosis caused by recurrent hemorrhage may show focal wall nodularity on sonography, and it is difficult for sonographers to differentiate these findings from malignant transformation with only a B- mode scan [20]. Doppler imaging may be helpful in detecting malignant transformation. Endometriomas do not show significant differences in flow indexes (resistive index and pulsatility index) compared with other benign cystic lesions [22]. However, once malignant transformation occurs, it may be that the resistive and pulsatility indexes change to show malignant patterns. However, no such findings have been reported to date. MR imaging can provide higher specificity in diagnosing endometriosis [17]. Therefore, patients with indeterminate sonographic findings and in whom there is a suspicion of endometriosis may benefit from MR imaging. Simple endometrial cysts benign neoplasms that develop from endometrial cysts and decidual change of the ectopic endometrium during pregnancy should be considered in the differential diagnosis. In endometrial cysts, blood clots on the cyst wall can be seen as mural nodules; however, they do not enhance [14, 15, 23]. Adenofibroma, which can develop in endometrial cysts, has been reported to show hypointense mural nodules, in contrast to hyperintense endometrioid adenocarcinomas [24]. However, we encountered two patients with adenocarcinoma in endometrioma in whom the mural nodules showed low signal intensity on T2-weighted images. Furthermore, adenofibroma of the uterus has been reported to mimic endometrial carcinoma [25]. Therefore, we speculate that benign neoplasms in endometrial cysts cannot be distinguished from adenocarcinoma. Decidual change of the ectopic endometrial tissue has also been reported to mimic malignant transformation [26]; it can also show mural nodules on the wall of endometrial cysts and is hard to distinguish from blood clots on MR imaging because contrast material is not used in pregnant patients. However, in our limited experience, MR imaging characteristics of mural nodules composed of deciduosis are slightly different from those of malignant transformation. They tend to appear multifocal and rectangular in shape. Nevertheless, it is necessary to investigate imaging findings of decidualized endometrial cysts to gain a better understanding. Unfortunately, our study has some limitations because of its retrospective nature, small sample size, and selection bias in the control group. MR imaging was performed with different equipment. Dynamic subtraction imaging was performed in only five patients. The control group was composed of patients with endometriosis and possible malignant transformation on sonography, and pathologic confirmation of benign endometrioma was obtained in only five of 10 control patients. On the basis of our 10 patients with ovarian carcinoma in endometriosis, we conclude that endometrial cysts with malignant transformation rarely show low signal intensity on T2-weighted MR images. They usually have enhancing nodules that are most clearly depicted on dynamic subtraction imaging. We recommend performing dynamic subtraction imaging when this uncommon entity is suspected. Acknowledgments We thank Hajime Tsunoda, Ken Nishide, Keiko Kohno, Sayuri Otani, and Hiroko Shimizu-Tsunoda for recruiting patients to undergo MR imaging. We also thank the radiologic technologists at our institute, especially Masashi Shindo, Yuji Hirano, and Nobuyoshi Fujisawa, for their endeavors to obtain precise MR images. References 1. D Hooghe TM, Hill JA. Endometriosis. In: Berek JS, Adashi EY, Hillard PA, eds. Novak s gynecology, 12th ed. Baltimore: Williams & Wilkins, 1996: Sampson JA. Endometrial carcinoma of the ovary, arising in endometrial tissue in that organ. Arch Surg 1925;10: Stevenson CS. Malignant transformation of ovarian endometriosis: nature, treatment, and report of two cases. Obstet Gynecol 1970;36: Heaps JM, Nieberg RK, Berek JS. Malignant neoplasms arising in endometriosis. Obstet Gynecol 1990;75: Tohya T, Shibata S, Fujisaki S, Maeyama M. Clear cell carcinoma and endometrioid carcinoma arising in a endometriotic cyst of the ovary. Acta Obstet Gynaecol Jpn 1986;38: McMeekin DS, Burger RA, Manetta A, DiSaia P, Berman ML. Endometrioid adenocarcinoma of the ovary and its relationship to endometriosis. Gynecol Oncol 1995;59: Chew S, Tham KF, Ratnam SS. A series of ovarian clear cell and endometrioid carcinoma and their association with endometriosis. Singapore Med J 1997;38: Vercellini P, Parazzini F, Bolis G, et al. Endometriosis and ovarian cancer. Am J Obstet Gynecol 1993;169: Jimbo H, Yoshikawa H, Onda T, Yasugi T, Sakamoto A, Taketani Y. Prevalence of ovarian endometriosis in epithelial ovarian cancer. Int J Gynaecol Obstet 1997;59: Weinfeld RM, Johnson SC, Lucas CE, Saksouk FA. CT diagnosis of perihepatic endometriosis complicated by malignant transformation. Abdom Imaging 1998;23: Stringfellow JM, Hawnaur JM. CT and MRI appearances of sarcomatous change in chronic pelvic endometriosis. Br J Radiol 1998;71: Scully RE, Barlow JF. Mesonephroma of ovary: tumor of Müllerian nature related to the endometrioid carcinoma. Cancer 1967;20: Corner GW Jr, Hu C, Hertig AT. Ovarian carcinoma arising in endometriosis. Am J Obstet Gynecol 1950;59: Fujiwara T, Sugimura K, Yoshizako T, Imaoka I, Kitao M. MR findings of two cases of endometrial carcinoma accompanied with endometrial cysts [in Japanese]. Jpn J Clin Radiol 1994;39: Nobusawa H, Munechika K, Kushima M, Gokan T, Ishikawa N. MR imaging of malignant tumor arised from the wall of endometrial cysts; report of two cases [in Japanese]. Jpn J Clin Radiol 1995;40: Nishimura K, Togashi K, Itoh K, et al. Endometrial cysts of the ovary: MR imaging. Radiology 1987; 162: Togashi K, Nishimura K, Kimura I, et al. Endometrial cysts: diagnosis with MR imaging. Radiology 1991;180: Ghossain MA, Buy JN, Ligneres C, et al. Epithelial tumors of the ovary: comparison of MR and CT findings. Radiology 1991;181: 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: Patel MD, Feldstein VA, Chen DC, Lipson SD, Filly RA. Endometriomas: diagnostic performance of US. Radiology 1999;210: Buy JN, Ghossain MA, Sciot C, et al. Epithelial tumors of the ovary: CT findings and correlation with US. Radiology 1991;178: Aleem F, Pennisi J, Zeitoun K, Predanic M. The role of color Doppler in diagnosis of endometriomas. Ultrasound Obstet Gynecol 1995;5: Togashi K, Konishi J. Magnetic resonance imaging in the evaluation of gynecologic malignancy. Magn Reson Q 1990;6: Matsuo Y, Doi J, Matsubayashi R, et al. Two cases of adenofibroma accompanied with endometrial cyst [in Japanese]. In: Nakamura H, ed. 12th annual meeting of the Japanese Society for Abdominal Radiology. Osaka, Japan: Japanese Society for Abdominal Radiology, 1998: Kaji Y, Sugimura K, Okizuka H. Uterine adenofibroma mimicking endometrial carcinoma: MR findings (letter). AJR 1992;158: Miyakoshi K, Tanaka M, Gabionza D, et al. Decidualized ovarian endometriosis mimicking malignancy. AJR 1998;171: AJR:175, November 2000

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