CASE REPORT
Magnetic Resonance Imaging Manifestations of Ovarian Mullerian Mixed Epithelial Borderline Tumors: Imaging and Histologic Features in Comparison With Mullerian Mucinous Borderline Tumors Roka Namoto Matsubayashi, MD, PhD,*† Yoshitomo Matsuo, MD,‡ Takahiko Nakazono, MD, PhD,§ Seiya Momosaki, MD, PhD,|| and Toru Muranaka, MD, PhD†¶ Abstract: We illustrate the magnetic resonance imaging features of 3 cases of rare ovarian Mullerian mixed epithelial borderline tumor (MEBT) and identify important diagnostic clues based on their detailed histologic, morphologic, and clinical features. Mullerian mixed epithelial borderline tumor has good prognosis, and adequate management is essential. In order to avoid unnecessary aggressive treatment, radiologists should become familiar with the imaging findings of MEBT. To the best of our knowledge, no articles have described the detailed images of MEBT. Key Words: Mullerian mixed epithelial borderline tumor, MRI, ovary, borderline tumor, endometriosis (J Comput Assist Tomogr 2015;39: 276–280)
M
ullerian mixed epithelial borderline tumor (MEBT) is one of the rare borderline tumors that account for 5% of all borderline tumors, and is first characterized in 1988 by Rutgers and Scully.1 I believe that it is a rare tumor, and radiologists may not be familiar with the disease concept of MEBT. However, it is important to accurately diagnose borderline tumors of the ovaries (BTOs) including MEBT in terms of fertility preservation. Borderline tumors of the ovaries have a relatively good prognosis and originate in younger patients compared with malignant tumors.2 In addition, these tumors frequently originate from or are associated with endometriotic cysts1,2 and are often observed in the bilateral ovaries. This finding is very important because the tumors often originate in patients of childbearing age; thus, the administration of careful and adequate treatment to spare the function of reproductive organs is required. Mullerian mixed epithelial borderline tumors are composed of the admixture of 2 or more of the following cell types: endocervicallike mucinous, ciliated serous, endometrioid, and squamous.1 The second or second and third cell types must comprise alone or together at least 10% of the neoplastic lining.3 The average patient age is young (35 years). A total of 53% of cases involve endometriosis, with 33% of cases involving endometriosis in the ipsilateral ovary.1 Macroscopically, MEBTs are bilateral in approximately 22% of cases. The tumor is often unilocular with intracystic papillae, which resembles those of Mullerian mucinous borderline tumors (MMBTs) and serous borderline tumors (SBTs).1 From the *Breast Care Center and †Department of Radiology, National Kyushu Medical Center, Jigyohama, Chuo-ku, Fukuoka, Japan; ‡e-Site Healthcare Company, Kandasuda-cho 1-chome, Chiyoda-ku, Tokyo, Japan; §Department of Radiology, Faculty of Medicine, Saga University, Saga, Japan; ∥Department of Pathology, and ¶Clinical Research Institute, National Kyushu Medical Center, Jigyohama, Chuo-ku, Fukuoka, Japan. Received for publication July 24, 2014; accepted October 17, 2014. Reprints: Roka Namoto Matsubayashi, MD, PhD, Breast Care Center and Department of Radiology, National Kyushu Medical Center, Jigyohama, Chuo-ku, Fukuoka, Japan (e‐mail: [email protected]; [email protected]). The authors declare no conflict of interest. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Mullerian mucinous borderline tumor was also first described in 1988 by Rutgers and Scully.4 Mullerian mucinous borderline tumors exhibit epithelial proliferation of endocervical (Mullerian) mucinous-type cells.2 The average patient age is 34 years.4 Mullerian mucinous borderline tumors are bilateral in approximately 40% of cases,5 and often unilocular with intracystic papillae. A total of 30% of cases involve endometriosis, with 20% of such cases involving endometriosis in the ipsilateral ovary. These clinical and histological features resembled those of MEBTs. In this article, we report 3 patients with MEBTs and describe the characteristics of MEBTs and discuss the essential diagnostic clues for diagnosing MEBT using magnetic resonance imaging (MRI). Detailed morphologic and histologic features as well as signal intensity (SI) characteristics on T2-weighted image (T2WI) and contrast-enhanced image (shape, fibrosis, edematous changes, SI, and enhancement patterns) are specifically described. In addition, the imaging findings are compared with those of MMBTs experienced at our institution and reported cases. To the best of our knowledge, no reports have thus far described the detailed imaging findings of MEBTs.
CASE REPORTS We experienced 3 cases of MEBTs between 2006 and 2011 (Table 1). The patients' ages were 67, 46, and 66 years (mean, 59 years) (Table 1). None of the patients had undergone chemotherapy or biopsy for tissue sampling before the magnetic resonance (MR) examination. Surgical treatment was performed in each case. The institutional review board approved this retrospective study, and therefore no individual patient consent was required. Written informed consent was obtained from each patient before surgical treatment.
Case 1 A 67-year-old woman detected a mass in her left ovary through abdominal ultrasonography. The mass is 6 cm in diameter with smooth surface. On MRI, the lesion exhibited polypoid papilla in the endometriotic cysts on MRI. The papilla displayed homogeneous low SI on T1-weighted image (T1WI) (not shown). On T2WI, the papilla showed very high SI on the surface/ periphery to background of the low-signal endometriotic cysts, with a low SI core (Fig. 1A, B). Weak enhancement of the papillae in the periphery was observed on dynamic contrast-enhanced studies (Fig. 1E). On the basis of these MRI findings, we diagnosed the mass as MEBT or MMBT. Left ovarian tumor resection was performed. Macroscopically, edematous changes severe enough to appear in cysts were observed on the surface of the tumor (Fig. 1C). Histologically, severe edematous branching papillae with a J Comput Assist Tomogr • Volume 39, Number 2, March/April 2015
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TABLE 1. Clinical Features of 3 Patients With MEBTs and 2 Patients With MMBTs Case Age, y Size of Mass, cm Affected Side Histologic Finding 1 2 3 4* 5*
67 46 66 42 38
3 5 2 4 7
Left Right Left Left Right
MEBT MEBT MEBT MMBT MMBT
*For the comparison of the imaging features of MEBTs, MMBTs (cases 4 and 5) are included.
fibrous core were noted (Fig. 1D). The high intensity on T2WI reflects an edematous stroma (Fig. 1B–D). The tumors showed finely branching complex papillae with detached cell clusters reminiscent of SBTs (not shown). The surface epithelia had been composed of the admixture of endocervical-like mucinous, ciliated serous, and endometrioid. Histological diagnosis was MEBT.
Case 2 A 46-year-old woman complained of abdominal distention and pain. The patient exhibited a polypoid papilla in the endometriotic cyst in the right ovary on MRI. The papillae displayed
MRI Manifestations of Ovarian MEBTs
homogeneous low SI on T1WI (not shown). On T2WI, the papilla has very high SI on the surface/periphery to background of the low-signal endometriotic cysts, with a low SI core (Fig. 2A). This patient has asthma; no contrast-enhanced study was performed. Histologically, severely edematous branching papillae with a fibrous core are noted (Fig. 2B). The surface epithelia had been composed of the admixture of endocervical-like mucinous, ciliated serous, and endometrioid. Right ovarian tumor resection was performed, and the histological diagnosis was MEBT.
Case 3 A 66-year-old woman detected a mass lesion in her left ovary through abdominal ultrasonography. The lesion is 7 cm in diameter with smooth surface. On MRI, the lesion exhibited as a polypoid papilla in the endometriotic cysts on MRI. The papilla displayed homogeneous low SI on T1WIs (not shown). On T2WIs, this papilla shows low SI with branching surface (Fig. 3A). In this case, a relatively high signal on T2WI in an endometriotic cyst and a high SI on the surface of the papillae were rather obscure; however, based on a detailed observation, the findings can be recognized (Fig. 3B). The morphological characteristics of the papillae were the same as those observed in the other 2 cases. Weak enhancement of the papilla was observed on dynamic contrast-enhanced studies (Fig. 3C). On the basis of these MRI findings, we diagnosed the mass as MEBT or MMBT.
FIGURE 1. Case 1. A 67-year-old woman with a left ovarian MEBT. The MEBT contains polypoid papillae in the endometriotic cyst (A). The papillae exhibit very high SI in the periphery with a low-SI core on T2WI [A (arrows) and B]. Macroscopically, edematous changes severe enough to appear in cysts are observed on the surface of the tumor (C). Histologically, severely edematous branching papillae with a fibrous core are noted (D). The high intensity on T2WI may reflect an edematous stroma. The endometriotic cyst demonstrates “shading” on T2WI, and peripheral high-intensity areas are clearly observed. Weak enhancement of the papillae in the periphery is detected on a dynamic contrast-enhanced study (E). © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 2. Case 2. A 46-year-old woman with a left ovarian MEBT. The MEBT exhibits polypoid papillae in the endometriotic cyst (A). These imaging features are similar to those observed in Figure 1. Histologically, severely edematous branching papillae with a fibrous core are noted (B).
Left ovarian tumor resection was performed, and the histological diagnosis was MEBT.
DISCUSSION A wide variety of ovarian tumors are classified based on histologic features. The ovaries consist of various tissues, including follicular cells, granulosa cells, the surface epithelium, and the ovarian cortex. Therefore, various tumors may originate from tissues in the ovaries. Most BTOs are cystic neoplasms with papillary excrescences or multicystic neoplasms that demonstrate epithelial proliferation with stratification and tufting but lack stromal invasion; these tumors usually behave in a benign fashion. Borderline tumors of the ovaries form a separate entity within the group of ovarian tumors acknowledged by the International Federation of Gynecology and Obstetrics in 1961 and adapted by the World Health Organization in 1973. Three terms are currently used to refer to these tumors: borderline tumors, tumors of low malignant potential, and atypical proliferative tumors. The radicality of surgical procedures, especially in younger patients for whom preserving fertility is an important consideration, the surgical staging and the type of operative approach (laparoscopy vs laparotomy) remain important topics of debate.5 Borderline tumors of the ovaries are present at an early stage and have a favorable prognosis.5 Borderline tumors of the ovaries are classified into 12 types according to the World Health Organization histological classification of tumors of the ovaries and account
for 9.2% to 16.3% of all nonbenign epithelial ovarian tumors,3 with an incidence of 1.8 to 4.8 per 100,000 women per year.5 Mullerian mixed epithelial borderline tumors are included in BTOs, and were first characterized in 1988.1 Histologically, the tumors are composed of papillae with detached cell clusters reminiscent of SBTs; however, they generally contain a mixture of endocervical-like cells and indifferent eosinophilic epithelium. Endometriotic cysts are seen in more than half of the cases of MEBT.1 On the other hand, MMBTs account for 10% to 15% among mucinous borderline tumors by 2 types of Mullerian type and intestinal type. Excluding the difference of covering epithelium, structural features of MEBT and MMBT closely resemble. Recently, MMBT has been familiar among radiologists. Because, several cases6 had been described about their imaging findings. Although MEBT is a similar entity in ovarian borderline tumors, awareness is low, and radiologists or general pathologists may not correctly recognize this tumor. Our presented cases especially cases 1 and 3 were older than reported cases, but the size of endometriotic cysts with MEBTs was large in these cases. Especially, internal SI of endometriotic cyst had changed in case 3. Tanaka et al7 reported that endometriotic cysts with tumors were large and there was different internal SI. The findings of our cases suggest that a certain period has elapsed since the tumor occurred. However, MEBTs are low-grade malignant tumors; therefore, the lesions might remain within the cysts even after a long period has elapsed. And then, one of our presented cases in our institution was initially diagnosed as an SBT. As in this case, I suppose there
FIGURE 3. Case 3. A 66-year-old woman with a left ovarian MEBT. The MEBT exhibits small polypoid papillae in the endometriotic cyst (A–C). In this case, the endometriotic cyst displays a relatively high SI compared to that observed in the other cases of MEBT (A and B). The high SI on the surface of the papillae is rather obscure; however, based on a detailed observation, the findings can be recognized (B). The morphological characteristics of the papillae are the same as those noted in the other cases. A tiny cyst is observed in the base of the papilla. Figure 3 can be viewed online in color at www.jcat.org.
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J Comput Assist Tomogr • Volume 39, Number 2, March/April 2015
MRI Manifestations of Ovarian MEBTs
FIGURE 4. A 42-year-old woman with a left ovarian MMBT. The MMBT exhibits polypoid papillae in the endometriotic cyst. The papillae display a very high SI with a delicate branching core on T2WI (A) (a “cotton ball-like” appearance) and weak enhancement on a contrast-enhanced study (B).
is a possibility that MEBT has been diagnosed with SBT pathologically. Therefore, the age distribution of real MEBT might be broader.
Comparison With the Characteristics of the MRI Findings of the MMBTs We experienced 2 cases of MMBT. On MRI, the patients with MMBTs exhibited polypoid papillae in the endometriotic cysts.
The papillae displayed low SI on T1WI (not shown) and very high SI on the surface, with a low SI core on T2WI (Figs. 4A and 5A) and weak enhancement on dynamic contrast studies (Figs. 4B and 5D). Macroscopically, the papillae demonstrated edematous changes in the surface, and histologically, branching edematous papillae lined by endocervical type mucinous cells were observed. Mucinous material was observed on the tumor surface; however, it was in small amount. The histologic characteristics (dense fibrosis of the stroma with severe edematous changes on the surface)
FIGURE 5. A 38-year-old woman with a left ovarian MMBT. The MMBT exhibits large papillae in the endometriotic cyst (A). The papillae display very high SI on T2WI with a low-SI core (A) and weak enhancement on a contrast-enhanced study (B). The endometriotic cyst demonstrates “shading” on T2WI (A). Histologically, branching edematous papillae lined by endocervical-type mucinous cells are observed (C and D). © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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TABLE 2. Correlations Between the MR Manifestations and Histological Features of MEBTs Imaging Features
Histologic Features
Polypoid papillae in the endometriotic cysts The papillae exhibit a very high SI on the surface with a low-SI core on T2WI (resembling that observed in MMBTs)
Polypoid papillae in the endometriotic cysts The branching stroma of the papillae on the surface exhibits severe edema and appears as cyst-like nodules The basal side of the stroma shows dense desmoplastic changes *These histological features are similar to those of MMBTs and SBTs.
*Due to shading on T2WI caused by endometriotic cysts, the high SI on the surface of papillae is more clear than that observed in SBTs. *As the features of the MEBTs, first mentioned important findings by this paper.
of papillae of MMBTs are similar to those of MEBTs. In the cases of MEBTs, due to shading of endometriotic cysts on T2WI, the high SI observed on the surface of the papillae was clear and it was an important characteristic finding for diagnosing MEBTs. As in the case of MEBTs, this finding is an important feature for diagnosing MMBTs. However, this feature has not been previously described in reports of MMBTs.6 A summary of the important diagnostic findings of MEBTs/ MMBTs is as follows: 1. MEBTs/MMBTs often contain polypoid papillae in the endometriotic cysts. 2. The papillae display very high SI on the surface/periphery to background of low-signal endometriotic cysts, with a branching core on T2WI (a “cotton ball-like” appearance) and weak enhancement on dynamic contrast-enhanced studies. 3. The high SI observed on T2WI may reflect a severely edematous stroma. 4. The imaging findings of MEBTs and MMBTs are similar.
Diagnostic Strategy Based on the Histologic/Morphologic Features of MEBTs Table 2 presents the detailed correlations between the MR manifestations and histologic features of MEBTs. The excrescences/papillae of MEBTs exhibit similar features to those of MMBTs, as their structure is composed of a fibrous branching stroma with peripheral edematous changes. However, especially in cases of MEBTs/MMBTs, the tumors often originate in endometriotic cysts, and, due to shading of the cysts on T2WI, peripheral high SI (edematous changes) is observed to be intense. Kataoka et al6 suggested that the high intensity of MMBT on T2WIs reflects the presence of intraluminal mucinous material and stromal edema; however, the present MEBTs exhibited similar imaging features on T2WI, and no mucinous materials were observed on the histologic specimens. The conclusion to be drawn here is that severe stromal edema primarily results in high SI. Furthermore, the morphological features of papillae in MEBTs/ MMBTs and the excrescences of SBTs are similar. Therefore, SBTs also may exhibit the high signal of the surface layer, but because the liquid contents of the cysts are also high signal, it is unclear. On the basis of the detailed interpretation, it is possible to find spotty high-signal areas on the surface of the excrescences. When diagnosing BTOs, it should be noted that these tumors often originate from or are associated with endometriotic cysts
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(especially MEBTs/MMBTs and endometrioid borderline tumors). Various carcinomas are associated with endometriotic cysts; typical examples include endometrioid carcinomas and clear-cell carcinomas. However, these tumors tend to be strongly enhanced, and the solid components are sessile. With the increase in incidence of late childbearing, preserving fertility is becoming more important. Even ovarian tumors with a solid component are not always malignant. Carefully determining and observing the precise form of the lesion is required.
CONCLUSIONS The MR finding of a cotton-ball appearance reflects the histologic characteristics of MEBT, which resemble those of MMBTs. With respect to diagnosis, the histologic features of intracystic papillae are the most notable findings for appropriately interpreting the MR characteristics of MEBTs. Furthermore, it is important to identify the clinical and imaging characteristics of MEBTs to distinguish these lesions from highly malignant tumors and prevent inadequate surgical treatment, especially in patients of childbearing age. In particular, performing a careful evaluation is highly recommended in cases of tumors associated with endometriosis. REFERENCES 1. Rutgers JL, Scully RE. Ovarian mixed-epithelial papillary cystadenomas of borderline malignancy of mullerian type. A clinicopathologic analysis. Cancer. 1988;61:546–554. 2. Burger CW, Prinssen HM, Baak JPA, et al. The management of borderline epithelial tumors of the ovary. Int J Gynecol Cancer. 2000;10:181–197. 3. Tavassoli F, Devilee P. World Health Organization Classification of Tumours. Pathology and Genetics Tumours of the Breast and Female Genital Organs. Lyon, France: IARC Press; 2003. 4. Rutgers JL, Scully RE. Ovarian mullerian mucinous papillary cystadenomas of borderline malignancy. A clinicopathologic analysis. Cancer. 1988;61: 340–348. 5. Fischerova D, Zikan M, Dundr P, et al. Diagnosis, treatment, and follow-up of borderline ovarian tumors. Oncologist. 2012;17:1515–1533. 6. Kataoka M, Togashi K, Koyama T, et al. MR imaging of müllerian mucinous borderline tumors arising from endometriotic cysts. J Comput Assist Tomogr. 2002;26:532–537. 7. Tanaka YO, Yoshizako T, Nishida M, et al. Ovarian carcinoma in patients with endometriosis: MR imaging findings. Am J Roentgenol. 2000;175: 1423–1430.
© 2015 Wolters Kluwer Health, Inc. All rights reserved.
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Magnetic Resonance Imaging Manifestations of Ovarian Mullerian Mixed Epithelial Borderline Tumors: Imaging and Histologic Features in Comparison With Mullerian Mucinous Borderline Tumors Roka Namoto Matsubayashi, MD, PhD,*† Yoshitomo Matsuo, MD,‡ Takahiko Nakazono, MD, PhD,§ Seiya Momosaki, MD, PhD,|| and Toru Muranaka, MD, PhD†¶ Abstract: We illustrate the magnetic resonance imaging features of 3 cases of rare ovarian Mullerian mixed epithelial borderline tumor (MEBT) and identify important diagnostic clues based on their detailed histologic, morphologic, and clinical features. Mullerian mixed epithelial borderline tumor has good prognosis, and adequate management is essential. In order to avoid unnecessary aggressive treatment, radiologists should become familiar with the imaging findings of MEBT. To the best of our knowledge, no articles have described the detailed images of MEBT. Key Words: Mullerian mixed epithelial borderline tumor, MRI, ovary, borderline tumor, endometriosis (J Comput Assist Tomogr 2015;39: 276–280)
M
ullerian mixed epithelial borderline tumor (MEBT) is one of the rare borderline tumors that account for 5% of all borderline tumors, and is first characterized in 1988 by Rutgers and Scully.1 I believe that it is a rare tumor, and radiologists may not be familiar with the disease concept of MEBT. However, it is important to accurately diagnose borderline tumors of the ovaries (BTOs) including MEBT in terms of fertility preservation. Borderline tumors of the ovaries have a relatively good prognosis and originate in younger patients compared with malignant tumors.2 In addition, these tumors frequently originate from or are associated with endometriotic cysts1,2 and are often observed in the bilateral ovaries. This finding is very important because the tumors often originate in patients of childbearing age; thus, the administration of careful and adequate treatment to spare the function of reproductive organs is required. Mullerian mixed epithelial borderline tumors are composed of the admixture of 2 or more of the following cell types: endocervicallike mucinous, ciliated serous, endometrioid, and squamous.1 The second or second and third cell types must comprise alone or together at least 10% of the neoplastic lining.3 The average patient age is young (35 years). A total of 53% of cases involve endometriosis, with 33% of cases involving endometriosis in the ipsilateral ovary.1 Macroscopically, MEBTs are bilateral in approximately 22% of cases. The tumor is often unilocular with intracystic papillae, which resembles those of Mullerian mucinous borderline tumors (MMBTs) and serous borderline tumors (SBTs).1 From the *Breast Care Center and †Department of Radiology, National Kyushu Medical Center, Jigyohama, Chuo-ku, Fukuoka, Japan; ‡e-Site Healthcare Company, Kandasuda-cho 1-chome, Chiyoda-ku, Tokyo, Japan; §Department of Radiology, Faculty of Medicine, Saga University, Saga, Japan; ∥Department of Pathology, and ¶Clinical Research Institute, National Kyushu Medical Center, Jigyohama, Chuo-ku, Fukuoka, Japan. Received for publication July 24, 2014; accepted October 17, 2014. Reprints: Roka Namoto Matsubayashi, MD, PhD, Breast Care Center and Department of Radiology, National Kyushu Medical Center, Jigyohama, Chuo-ku, Fukuoka, Japan (e‐mail: [email protected]; [email protected]). The authors declare no conflict of interest. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Mullerian mucinous borderline tumor was also first described in 1988 by Rutgers and Scully.4 Mullerian mucinous borderline tumors exhibit epithelial proliferation of endocervical (Mullerian) mucinous-type cells.2 The average patient age is 34 years.4 Mullerian mucinous borderline tumors are bilateral in approximately 40% of cases,5 and often unilocular with intracystic papillae. A total of 30% of cases involve endometriosis, with 20% of such cases involving endometriosis in the ipsilateral ovary. These clinical and histological features resembled those of MEBTs. In this article, we report 3 patients with MEBTs and describe the characteristics of MEBTs and discuss the essential diagnostic clues for diagnosing MEBT using magnetic resonance imaging (MRI). Detailed morphologic and histologic features as well as signal intensity (SI) characteristics on T2-weighted image (T2WI) and contrast-enhanced image (shape, fibrosis, edematous changes, SI, and enhancement patterns) are specifically described. In addition, the imaging findings are compared with those of MMBTs experienced at our institution and reported cases. To the best of our knowledge, no reports have thus far described the detailed imaging findings of MEBTs.
CASE REPORTS We experienced 3 cases of MEBTs between 2006 and 2011 (Table 1). The patients' ages were 67, 46, and 66 years (mean, 59 years) (Table 1). None of the patients had undergone chemotherapy or biopsy for tissue sampling before the magnetic resonance (MR) examination. Surgical treatment was performed in each case. The institutional review board approved this retrospective study, and therefore no individual patient consent was required. Written informed consent was obtained from each patient before surgical treatment.
Case 1 A 67-year-old woman detected a mass in her left ovary through abdominal ultrasonography. The mass is 6 cm in diameter with smooth surface. On MRI, the lesion exhibited polypoid papilla in the endometriotic cysts on MRI. The papilla displayed homogeneous low SI on T1-weighted image (T1WI) (not shown). On T2WI, the papilla showed very high SI on the surface/ periphery to background of the low-signal endometriotic cysts, with a low SI core (Fig. 1A, B). Weak enhancement of the papillae in the periphery was observed on dynamic contrast-enhanced studies (Fig. 1E). On the basis of these MRI findings, we diagnosed the mass as MEBT or MMBT. Left ovarian tumor resection was performed. Macroscopically, edematous changes severe enough to appear in cysts were observed on the surface of the tumor (Fig. 1C). Histologically, severe edematous branching papillae with a J Comput Assist Tomogr • Volume 39, Number 2, March/April 2015
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J Comput Assist Tomogr • Volume 39, Number 2, March/April 2015
TABLE 1. Clinical Features of 3 Patients With MEBTs and 2 Patients With MMBTs Case Age, y Size of Mass, cm Affected Side Histologic Finding 1 2 3 4* 5*
67 46 66 42 38
3 5 2 4 7
Left Right Left Left Right
MEBT MEBT MEBT MMBT MMBT
*For the comparison of the imaging features of MEBTs, MMBTs (cases 4 and 5) are included.
fibrous core were noted (Fig. 1D). The high intensity on T2WI reflects an edematous stroma (Fig. 1B–D). The tumors showed finely branching complex papillae with detached cell clusters reminiscent of SBTs (not shown). The surface epithelia had been composed of the admixture of endocervical-like mucinous, ciliated serous, and endometrioid. Histological diagnosis was MEBT.
Case 2 A 46-year-old woman complained of abdominal distention and pain. The patient exhibited a polypoid papilla in the endometriotic cyst in the right ovary on MRI. The papillae displayed
MRI Manifestations of Ovarian MEBTs
homogeneous low SI on T1WI (not shown). On T2WI, the papilla has very high SI on the surface/periphery to background of the low-signal endometriotic cysts, with a low SI core (Fig. 2A). This patient has asthma; no contrast-enhanced study was performed. Histologically, severely edematous branching papillae with a fibrous core are noted (Fig. 2B). The surface epithelia had been composed of the admixture of endocervical-like mucinous, ciliated serous, and endometrioid. Right ovarian tumor resection was performed, and the histological diagnosis was MEBT.
Case 3 A 66-year-old woman detected a mass lesion in her left ovary through abdominal ultrasonography. The lesion is 7 cm in diameter with smooth surface. On MRI, the lesion exhibited as a polypoid papilla in the endometriotic cysts on MRI. The papilla displayed homogeneous low SI on T1WIs (not shown). On T2WIs, this papilla shows low SI with branching surface (Fig. 3A). In this case, a relatively high signal on T2WI in an endometriotic cyst and a high SI on the surface of the papillae were rather obscure; however, based on a detailed observation, the findings can be recognized (Fig. 3B). The morphological characteristics of the papillae were the same as those observed in the other 2 cases. Weak enhancement of the papilla was observed on dynamic contrast-enhanced studies (Fig. 3C). On the basis of these MRI findings, we diagnosed the mass as MEBT or MMBT.
FIGURE 1. Case 1. A 67-year-old woman with a left ovarian MEBT. The MEBT contains polypoid papillae in the endometriotic cyst (A). The papillae exhibit very high SI in the periphery with a low-SI core on T2WI [A (arrows) and B]. Macroscopically, edematous changes severe enough to appear in cysts are observed on the surface of the tumor (C). Histologically, severely edematous branching papillae with a fibrous core are noted (D). The high intensity on T2WI may reflect an edematous stroma. The endometriotic cyst demonstrates “shading” on T2WI, and peripheral high-intensity areas are clearly observed. Weak enhancement of the papillae in the periphery is detected on a dynamic contrast-enhanced study (E). © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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FIGURE 2. Case 2. A 46-year-old woman with a left ovarian MEBT. The MEBT exhibits polypoid papillae in the endometriotic cyst (A). These imaging features are similar to those observed in Figure 1. Histologically, severely edematous branching papillae with a fibrous core are noted (B).
Left ovarian tumor resection was performed, and the histological diagnosis was MEBT.
DISCUSSION A wide variety of ovarian tumors are classified based on histologic features. The ovaries consist of various tissues, including follicular cells, granulosa cells, the surface epithelium, and the ovarian cortex. Therefore, various tumors may originate from tissues in the ovaries. Most BTOs are cystic neoplasms with papillary excrescences or multicystic neoplasms that demonstrate epithelial proliferation with stratification and tufting but lack stromal invasion; these tumors usually behave in a benign fashion. Borderline tumors of the ovaries form a separate entity within the group of ovarian tumors acknowledged by the International Federation of Gynecology and Obstetrics in 1961 and adapted by the World Health Organization in 1973. Three terms are currently used to refer to these tumors: borderline tumors, tumors of low malignant potential, and atypical proliferative tumors. The radicality of surgical procedures, especially in younger patients for whom preserving fertility is an important consideration, the surgical staging and the type of operative approach (laparoscopy vs laparotomy) remain important topics of debate.5 Borderline tumors of the ovaries are present at an early stage and have a favorable prognosis.5 Borderline tumors of the ovaries are classified into 12 types according to the World Health Organization histological classification of tumors of the ovaries and account
for 9.2% to 16.3% of all nonbenign epithelial ovarian tumors,3 with an incidence of 1.8 to 4.8 per 100,000 women per year.5 Mullerian mixed epithelial borderline tumors are included in BTOs, and were first characterized in 1988.1 Histologically, the tumors are composed of papillae with detached cell clusters reminiscent of SBTs; however, they generally contain a mixture of endocervical-like cells and indifferent eosinophilic epithelium. Endometriotic cysts are seen in more than half of the cases of MEBT.1 On the other hand, MMBTs account for 10% to 15% among mucinous borderline tumors by 2 types of Mullerian type and intestinal type. Excluding the difference of covering epithelium, structural features of MEBT and MMBT closely resemble. Recently, MMBT has been familiar among radiologists. Because, several cases6 had been described about their imaging findings. Although MEBT is a similar entity in ovarian borderline tumors, awareness is low, and radiologists or general pathologists may not correctly recognize this tumor. Our presented cases especially cases 1 and 3 were older than reported cases, but the size of endometriotic cysts with MEBTs was large in these cases. Especially, internal SI of endometriotic cyst had changed in case 3. Tanaka et al7 reported that endometriotic cysts with tumors were large and there was different internal SI. The findings of our cases suggest that a certain period has elapsed since the tumor occurred. However, MEBTs are low-grade malignant tumors; therefore, the lesions might remain within the cysts even after a long period has elapsed. And then, one of our presented cases in our institution was initially diagnosed as an SBT. As in this case, I suppose there
FIGURE 3. Case 3. A 66-year-old woman with a left ovarian MEBT. The MEBT exhibits small polypoid papillae in the endometriotic cyst (A–C). In this case, the endometriotic cyst displays a relatively high SI compared to that observed in the other cases of MEBT (A and B). The high SI on the surface of the papillae is rather obscure; however, based on a detailed observation, the findings can be recognized (B). The morphological characteristics of the papillae are the same as those noted in the other cases. A tiny cyst is observed in the base of the papilla. Figure 3 can be viewed online in color at www.jcat.org.
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J Comput Assist Tomogr • Volume 39, Number 2, March/April 2015
MRI Manifestations of Ovarian MEBTs
FIGURE 4. A 42-year-old woman with a left ovarian MMBT. The MMBT exhibits polypoid papillae in the endometriotic cyst. The papillae display a very high SI with a delicate branching core on T2WI (A) (a “cotton ball-like” appearance) and weak enhancement on a contrast-enhanced study (B).
is a possibility that MEBT has been diagnosed with SBT pathologically. Therefore, the age distribution of real MEBT might be broader.
Comparison With the Characteristics of the MRI Findings of the MMBTs We experienced 2 cases of MMBT. On MRI, the patients with MMBTs exhibited polypoid papillae in the endometriotic cysts.
The papillae displayed low SI on T1WI (not shown) and very high SI on the surface, with a low SI core on T2WI (Figs. 4A and 5A) and weak enhancement on dynamic contrast studies (Figs. 4B and 5D). Macroscopically, the papillae demonstrated edematous changes in the surface, and histologically, branching edematous papillae lined by endocervical type mucinous cells were observed. Mucinous material was observed on the tumor surface; however, it was in small amount. The histologic characteristics (dense fibrosis of the stroma with severe edematous changes on the surface)
FIGURE 5. A 38-year-old woman with a left ovarian MMBT. The MMBT exhibits large papillae in the endometriotic cyst (A). The papillae display very high SI on T2WI with a low-SI core (A) and weak enhancement on a contrast-enhanced study (B). The endometriotic cyst demonstrates “shading” on T2WI (A). Histologically, branching edematous papillae lined by endocervical-type mucinous cells are observed (C and D). © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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TABLE 2. Correlations Between the MR Manifestations and Histological Features of MEBTs Imaging Features
Histologic Features
Polypoid papillae in the endometriotic cysts The papillae exhibit a very high SI on the surface with a low-SI core on T2WI (resembling that observed in MMBTs)
Polypoid papillae in the endometriotic cysts The branching stroma of the papillae on the surface exhibits severe edema and appears as cyst-like nodules The basal side of the stroma shows dense desmoplastic changes *These histological features are similar to those of MMBTs and SBTs.
*Due to shading on T2WI caused by endometriotic cysts, the high SI on the surface of papillae is more clear than that observed in SBTs. *As the features of the MEBTs, first mentioned important findings by this paper.
of papillae of MMBTs are similar to those of MEBTs. In the cases of MEBTs, due to shading of endometriotic cysts on T2WI, the high SI observed on the surface of the papillae was clear and it was an important characteristic finding for diagnosing MEBTs. As in the case of MEBTs, this finding is an important feature for diagnosing MMBTs. However, this feature has not been previously described in reports of MMBTs.6 A summary of the important diagnostic findings of MEBTs/ MMBTs is as follows: 1. MEBTs/MMBTs often contain polypoid papillae in the endometriotic cysts. 2. The papillae display very high SI on the surface/periphery to background of low-signal endometriotic cysts, with a branching core on T2WI (a “cotton ball-like” appearance) and weak enhancement on dynamic contrast-enhanced studies. 3. The high SI observed on T2WI may reflect a severely edematous stroma. 4. The imaging findings of MEBTs and MMBTs are similar.
Diagnostic Strategy Based on the Histologic/Morphologic Features of MEBTs Table 2 presents the detailed correlations between the MR manifestations and histologic features of MEBTs. The excrescences/papillae of MEBTs exhibit similar features to those of MMBTs, as their structure is composed of a fibrous branching stroma with peripheral edematous changes. However, especially in cases of MEBTs/MMBTs, the tumors often originate in endometriotic cysts, and, due to shading of the cysts on T2WI, peripheral high SI (edematous changes) is observed to be intense. Kataoka et al6 suggested that the high intensity of MMBT on T2WIs reflects the presence of intraluminal mucinous material and stromal edema; however, the present MEBTs exhibited similar imaging features on T2WI, and no mucinous materials were observed on the histologic specimens. The conclusion to be drawn here is that severe stromal edema primarily results in high SI. Furthermore, the morphological features of papillae in MEBTs/ MMBTs and the excrescences of SBTs are similar. Therefore, SBTs also may exhibit the high signal of the surface layer, but because the liquid contents of the cysts are also high signal, it is unclear. On the basis of the detailed interpretation, it is possible to find spotty high-signal areas on the surface of the excrescences. When diagnosing BTOs, it should be noted that these tumors often originate from or are associated with endometriotic cysts
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(especially MEBTs/MMBTs and endometrioid borderline tumors). Various carcinomas are associated with endometriotic cysts; typical examples include endometrioid carcinomas and clear-cell carcinomas. However, these tumors tend to be strongly enhanced, and the solid components are sessile. With the increase in incidence of late childbearing, preserving fertility is becoming more important. Even ovarian tumors with a solid component are not always malignant. Carefully determining and observing the precise form of the lesion is required.
CONCLUSIONS The MR finding of a cotton-ball appearance reflects the histologic characteristics of MEBT, which resemble those of MMBTs. With respect to diagnosis, the histologic features of intracystic papillae are the most notable findings for appropriately interpreting the MR characteristics of MEBTs. Furthermore, it is important to identify the clinical and imaging characteristics of MEBTs to distinguish these lesions from highly malignant tumors and prevent inadequate surgical treatment, especially in patients of childbearing age. In particular, performing a careful evaluation is highly recommended in cases of tumors associated with endometriosis. REFERENCES 1. Rutgers JL, Scully RE. Ovarian mixed-epithelial papillary cystadenomas of borderline malignancy of mullerian type. A clinicopathologic analysis. Cancer. 1988;61:546–554. 2. Burger CW, Prinssen HM, Baak JPA, et al. The management of borderline epithelial tumors of the ovary. Int J Gynecol Cancer. 2000;10:181–197. 3. Tavassoli F, Devilee P. World Health Organization Classification of Tumours. Pathology and Genetics Tumours of the Breast and Female Genital Organs. Lyon, France: IARC Press; 2003. 4. Rutgers JL, Scully RE. Ovarian mullerian mucinous papillary cystadenomas of borderline malignancy. A clinicopathologic analysis. Cancer. 1988;61: 340–348. 5. Fischerova D, Zikan M, Dundr P, et al. Diagnosis, treatment, and follow-up of borderline ovarian tumors. Oncologist. 2012;17:1515–1533. 6. Kataoka M, Togashi K, Koyama T, et al. MR imaging of müllerian mucinous borderline tumors arising from endometriotic cysts. J Comput Assist Tomogr. 2002;26:532–537. 7. Tanaka YO, Yoshizako T, Nishida M, et al. Ovarian carcinoma in patients with endometriosis: MR imaging findings. Am J Roentgenol. 2000;175: 1423–1430.
© 2015 Wolters Kluwer Health, Inc. All rights reserved.
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
