- Email: [email protected]
MRI of gynecological neoplasm
Journal of Clinical Imaging 28 (2004) 143 – 152
MRI of gynecological neoplasm Margaret H. Pui a,*, Qiu Yan Wang b, Bin Xu b, Guo Ping Fan b a
Department of Radiology, McMaster University Medical Center, PO Box 2000 Station A, Hamilton, Ontario, Canada L8N 3Z5 b Department of Radiology, Xin Hua Hospital, 1665 Kong Jiang Road, Shanghai, People’s Republic of China Received 1 March 2003; accepted 27 March 2003
Abstract MRI is multiplanar, has large field of view, superior contrast resolution and no known adverse effect on the reproductive potential of ovaries. It is useful for characterizing solid, cystic or necrotic tissue, blood and fat. Contrast-enhanced MRI is also a comprehensive examination of the entire pelvis including lymph nodes, peritoneum, pelvic sidewalls, bone and muscles. It provides information about areas difficult to assess surgically, can refine staging classification, assists in planning surgery or radiotherapy and may be more costeffective by limiting use of surgery. This is a pictorial essay of MRI assessment of female pelvic neoplasm. D 2004 Elsevier Inc. All rights reserved. Index terms: Magnetic resonance imaging; Pelvic tumor; Ovarian tumor; Uterine tumor; Adnexal mass
1. Introduction Transvaginal ultrasound can differentiate between functional cyst, dermoid, some endometriomas, abscess, hydrosalpinx, polycystic ovary and ectopic pregnancy. Because MRI is multiplanar, has large field of view, superior contrast resolution and no known adverse effect on the reproductive potential of ovaries, it is useful for characterizing indeterminate masses. Contrast-enhanced MRI is also a comprehensive examination of the entire pelvis including lymph nodes, peritoneum, pelvic sidewalls, bone and muscles. This is a pictorial essay of MRI assessment of female pelvic neoplasm.
2. Methods Of 140 female patients who underwent MRI investigation of pelvic disease from 1997 through 2001, histological confirmation was obtained in 90 patients (age range: 0.1 –81 years, average: 51.8 years) by surgical excision. Benign lesions included 12 uterine fibroids, 2 cervical polyps, 12 teratomas, 7 cystadenomas, 6 serous cysts, 7
endometriomas of the ovary and 5 pelvic abscesses. The malignant uterine tumors included seven endometrial carcinomas, five cervical carcinomas, one recurrent endometrial stromal sarcoma and one recurrent mixed mu¨llerian tumor. Ovarian malignancy included eight recurrent carcinomas, four serous cystadenocarcinomas, four metastases, three theca cell tumors, one granulosa cell tumor, one yolk sac tumor and one non-Hodgkin’s lymphoma. There were also one each of primary fallopian tube carcinoma and metastases of vagina and peritoneum. In all patients, sagittal, axial and coronal unenhanced turbo spin – echo T2-weighted images (TR/TE/number of acquisitions/echo train length; 3050/150/6/32) and turbo spin – echo T1weighted images (450/10/4/4) before and after intravenous injection of 20 mmol/kg of gadolinium – DTPA were acquired using a 0.5-T MR system. Sixteen images of 6-mm thickness and 0.6-mm interslice gap were obtained with 28 35 cm field of view, 192 256 matrix and acquisition time of 3 min 47 s. The images were reviewed by two radiologists (MHP, QYW) and correlated with histological diagnosis.
3. Discussion * Corresponding author. Tel.: +1-905-521-2100x73200; fax: +1-905522-1390. E-mail address: [email protected] (M.H. Pui). 0899-7071/04/$ – see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/S0899-7071(03)00116-5
MRI has high soft tissue contrast and is useful for characterization of solid, cystic or necrotic tissue, blood
144
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
and fat. It is also helpful for differential diagnosis of endometrial pathology in women who have obliterated cervical canal and unsuccessful dilatation and curettage or endometrial biopsy. MRI provides information about areas difficult to assess surgically including the dome of diaphragm, retroperitoneum and colon. It can refine staging classification and assist in planning surgery or radiotherapy. Exploratory laparotomy has accuracy of 73% compared to 97% accuracy of MRI for assessing depth of myometrial invasion and tumor volume. However,
microscopic peritoneal disease and large pelvic mass distorting anatomic landmark can decrease the staging accuracy to 75% [1 – 4]. Because of the two- to eightfold increased cost of laparoscopy, hysteroscopy, laparotomy and vaginal hysterectomy, and more than half of the suspicious pelvic masses by clinical examination, elevated CA 125 level and ultrasonography are benign, MRI may be more cost-effective by limiting use of surgery. Tumor spill from cyst rupture during laparoscopy or surgery can also be avoided [1,2].
Fig. 1. An 18-year-old girl with ovarian teratoma. (A) Axial T1-, (B) sagittal fat-saturated T2- and (C) sagittal enhanced T1-weighted images show a multilocular complex mass posterior and superior to the normal uterus (arrow). The mass has mixed cystic and solid components with variable signal intensities. The fat content (*) of the tumor immediately posterior to the uterus has high T1 signal and is suppressed on the fat-saturated T2-weighted image. There is moderate contrast enhancement in a portion of the solid tissue posterior to the fat.
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
145
Fig. 2. A 38-year-old woman with multiple large leiomyomas in the posterior uterine wall and fundus extending to the diaphragm. These tumors have welldefined margins with heterogeneous low to intermediate signals on sagittal T2-weighted image (A). The solid tumors (arrow) enhance homogeneously similar to the normal myometrium on the enhanced sagittal T1-weighted image (B). There is central cystic degeneration with T2 hyperintensity and no contrast enhancement.
Normal uterus and ovary have homogeneous intermediate T1 signal intensity on MRI. The uterine corpus has a T2-hyperintense central endometrium, T2-hypointense junctional zone of 3– 10 mm thickness and peripheral myometrium of intermediate T2 signal intensity. The junctional zone is a portion of the myometrium with different blood flow or hydration. The cervix has higher fibrous content with two or three zones of different signal intensities that are lower than the corpus. There is homogeneous contrast enhancement in the endometrium and peripheral myometrium greater than the junctional zone (Fig. 1). Normal ovary has low to intermediate T2 signal with T2-hyperintense follicles in the cortical and subcortical locations [2,5]. Endometrial thickening may represent submucosal leiomyoma, endometrial polyp or hyperplasia, mixed mesenchymal tumor or stromal tumor. Leiomyomas are typically well circumscribed and have low to intermediate T2 signals (Fig. 2). Endometrial polyps are benign nodular protrusions consisting of irregularly distributed endometrial glands, thick-walled blood vessels and dense fibrous or smooth muscle stroma. Polyps have intermediate T1 and heterogeneous high T2 signals. Large polyps distend the endometrial cavity, whereas small polyps blend with the endometrium and are not visible on MRI [6]. Both cases of cervical polyps in our review were not detected on MRI. Adenomatous hyperplasia and hyperplasia with atypia are considered
precancerous. The endometrial thickening is probably benign if high T2 signal and strong contrast enhancement are detected.
Fig. 3. A 66-year-old woman with endometrial carcinoma. Sagittal T2-weighted image demonstrates a 4-cm slightly hyperintense mass (*) in the endometrial cavity invading the junctional zone.
146
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
Fig. 4. Enhanced sagittal T1-weighted image shows mildly enhancing endometrial carcinoma infiltrating the myometrium and posterior bladder wall in a 72-year-old woman.
Fig. 6. A 67-year-old woman with recurrent mixed mu¨llerian tumor. (A) Axial T2-weighted image shows a 10-cm irregular mass with heterogeneous intermediate signal intensity (arrow). There is heterogeneous contrast enhancement of the tumor and ascites on the enhanced sagittal T1-weighted image (B).
Fig. 5. A 46-year-old woman with papillary adenocarcinoma of cervix. (A) Sagittal T2- and (B) enhanced T1-weighted images show a 5-cm cervical mass (arrow) with slightly higher T2 signal than normal myometrium and mild contrast enhancement.
Malignancy is suspected if the endometrial lesion has low to intermediate T2 signal, shows weak contrast enhancement and invades the junctional zone. These criteria have sensitivity of 50 –83%, specificity of 92– 97% and accuracy of 82– 89% for differentiating malignant from benign lesions [7]. Endometrial carcinoma is the most frequent malignant neoplasm of female genital tract (Figs. 3 and 4). It occurs mainly in peri- or postmenopausal women with peak age of 55 – 66 years. Adenocarcinoma accounts for 60 – 70%, adenocanthoma and adenosquamous carcinoma constitute 20– 30%, whereas clear cell, mucinous, secretory and papillary serous carcinomas are uncommon (Fig. 5). Sarcomas constitute 1 –3% of uterine malignancy including mixed mu¨llerian tumor (40 – 70%), leiomyosarcoma (40 – 50%), rhabdomyosarcoma and endometrial stromal sarcoma ( < 10%). Endometrial stromal sarcoma is more common in postmenopausal women with previous pelvic radiotherapy
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
147
Fig. 7. Recurrent endometrial stromal sarcoma in a 69-year-old woman presents as a large lobulated mass (arrow) posterior to the urinary bladder. The tumor has heterogeneous low to intermediate signals on the (A) sagittal T1- and (B) T2-weighted images.
(4– 38%). Clinical presentation of uterine malignancy is late with nonspecific symptoms of vaginal bleeding, pelvic pain or fullness, and sometimes passage of malignant tumor fragments. The sarcomas are heterogeneous masses with low to intermediate T1 and T2 signals and a few pockets of necrosis and bleed with T2 hyperintensities (Figs. 6 and 7). The prognosis and treatment depend on histological grading, nodal metastasis and
extent of myometrial invasion [1]. Mixed mu¨llerian tumors have mixed adenocarcinoma and rhabdomyosarcoma components. Endometrial stromal sarcoma derives from totipotential endometrial stromal cell. Preserved bundles of myometrial fibers are separated by clusters of tumor cells with abundant tumor vessels and prominent involvement of lymphatics and blood vessels. The tumor may be seen as scattered nodules, well-demarcated expansile
Fig. 8. A 52-year-old woman with mucinous cystadenoma of the right ovary. (A) Sagittal T2-weighted image shows a 10-cm septated cystic mass (arrow) with varying fluid signal intensities. The thin septa and cyst wall enhance with contrast on enhanced sagittal T1-weighted image (B).
148
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
Fig. 10. A 15-cm endometrioid adenocarcinoma of the ovary in a 68-yearold woman appears as a solid lobulated mass (arrow) with intermediate T2 signal and small amount of necrosis on (A) sagittal T2-weighted image. (B) Enhanced axial T1-weighted image shows mild homogeneous contrast enhancement and ascites.
Fig. 9. A 44-year-old woman with left ovarian serous papillary cystadenocarcinoma. (A) Axial T1-, (B) T2- and (C) enhanced T1-weighted images show a 9-cm septated cystic mass with multiple enhancing solid mural nodules. The cysts have varying signal intensities caused by hemorrhage and increased protein content.
polypoid mass expanding the endometrial cavity and disrupting the junctional zone, or poorly demarcated diffuse endometrial thickening with irregular junctional zone [8– 11]. Ovarian tumors may arise from surface epithelium (90%), germ cell or stroma. They are often benign (80%) and involve women of reproductive age. Common benign tumors are teratomas, serous and mucinous epithelial tumors. Cystic teratoma consists of cyst lined by epithelium resembling keratinized epidermis with sebaceous and sweat glands, palm-tree-like protrusion and round nodules due to mixture of hair and desquamated epithelial cells. The cyst fluid is rich in protein, has high viscosity and has high T2 signal. Layered debris may be seen due to matted hair with intermediate signal intensity
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
149
Fig. 11. A 60-year-old woman with recurrent clear cell carcinoma of the right ovary and ascites. (A) Axial T1- and (B) T2-weighted images show a 9-cm complex mass (arrowheads) with hemorrhage into both the septated cystic and solid components.
between fat and fluid. MRI has higher accuracy (93%) than ultrasound (86%) in characterizing teratoma (Fig. 1). The fatty content can be detected by chemical shift artifact and fat suppression [2,12 – 15]. Mucinous cystadenomas are multilocular cysts with varying signal intensities, uniform thin septa and wall (Fig. 8). Serous
cystadenomas are unilocular with fluid signal intensity similar to urine. Ovarian malignancy is more common in women older than 45 years of age. Because malignancy presents with minor symptoms of abdominal distention or pressure, 75% of the tumors are Stage II and 60% greater than Stage III
Fig. 12. A 2-month-old infant with a 10-cm yolk sac tumor of the ovary. The tumor displaces the uterus anteriorly (arrow) and has heterogeneous low T1 and high T2 signals on (A) sagittal T1- and (B) T2-weighted images. There is tumor infiltration of the bone marrow with T2 hyperintensity in the L5 vertebra and sacrum relative to the normal L4 vertebral body. The tumor extends to the sacral canal (*).
150
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
germinomas, yolk sac tumors and immature teratomas. Dysgerminomas are solid with hypointense fibrovascular septa and prominent enhancement. Malignant yolk sac tumors are mainly solid with hemorrhage and T2-hyperintense stromal edema (Fig. 12). They are hypervascular with signal voids and enhance more than myometrium [18]. Granulosa cell tumor of the ovary is an estrogen-producing sex and stromal cell tumor. It constitutes less than 10% of ovarian malignancy. It is solid with variable amount of cystic component and blood (Fig. 13). The uterus is enlarged with thick endometrium [19]. Thecoma and fibrothecoma have similar MRI appearance as granulosa cell tumor (Fig. 14). Krukenberg tumors constitute 5 – 10% of ovarian tumors. They commonly result from transcoelomic spread of colonic and gastric carcinoma penetrating the ovary and stimulating dense stromal reaction. Carcinoma of the breast, pancreas, gall bladder, lung and melanoma can
Fig. 13. A 51-year-old woman with granulosa cell tumor. (A) Axial T2- and (B) enhanced T1-weighted images show enlarged left ovary (arrow) with similar T2 signal intensity and contrast enhancement relative to the myometrium. There is central tumor necrosis and thick endometrium (*).
at diagnosis with 5-year survival rates of 80% and 5%, respectively. MRI is 95% sensitive, 89% specific and 96% accurate in differentiating benign from malignant adnexal masses [16]. Criteria for malignancy include large size greater than 4 cm, wall or septal thickness more than 3 mm, nodularity, vegetation or large solid component, necrosis or bleed, rapid and marked contrast enhancement, extension to adjacent organ or sidewall, peritoneal, mesenteric or omental disease, massive ascites and lymphadenopathy [4,16,17]. Epithelial ovarian carcinoma constitutes 85 –90% of all ovarian malignancy and includes serous, mucinous, endometrioid, clear cell and anaplastic carcinomas [2]. Serous papillary carcinoma is the most common and often has papillary projection and cyst content of variable signal intensity (Fig. 9). Endometrioid carcinoma and clear cell carcinoma present as unilocular cysts with nodule (Figs. 10 and 11). Malignant germ cell tumors of the ovary are dys-
Fig. 14. A 66-year-old woman with left ovarian theca cell tumor and ascites. (A) Sagittal T2-weighted image shows tumor mass posterior to the uterus. The tumor has lobulated margins, intermediate T2 signal and small pockets of necrosis. There is less contrast enhancement than the normal myometrium demonstrated on the enhanced axial T1-weighted image (B).
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
151
also metastasize to the ovaries. Ovarian metastases are often bilateral (60 – 80%) and solid (63%) with welldefined margin and preserved ovarian configuration. They have heterogeneous low to intermediate T1 signals. Half of the tumors have low T2 signals and moderate contrast enhancement because of dense collagenous stroma (Fig. 15). Mucin produced by the signet ring cells result in areas of high T2 signal. Ovarian metastases can be detected before the primary tumor is identified [20,21]. Ovarian lymphoma may be a local manifestation of occult lymph nodal disease or secondary site of systemic disease. Non-Hodgkin’s lymphoma accounts for less than 1% of primary ovary malignancy. It presents as a solid mass with homogeneous low to intermediate T1 signal intensity, slightly high T2 signal and mild to moderate contrast enhancement (Fig. 16). It is often bilateral, lobulated
Fig. 16. A 49-year-old woman with non-Hodgkin’s lymphoma of the left ovary. (A) Axial T1- and (B) T2-weighted images show a 3-cm lobular solid mass with homogeneous intermediate signals (arrow). There was mild contrast enhancement and associated left iliac and inguinal lymphadenopathy (not shown).
and associated with generalized lymphadenopathy or multiple lesions in other organs [22].
References
Fig. 15. A 68-year-old woman with ovarian metastases from gastric carcinoma. (A) Axial T2- and (B) enhanced T1-weighted images show a large ovary with preservation of normal ovarian configuration (arrow). The tumor has intermediate T1 and T2 signals and heterogeneous contrast enhancement.
[1] Sacz F, Urresola A, Larena JA, Martin JI, Pijuan JI, Schneider J, Ibanez E. Endometrial carcinoma: assessment of myometrial invasion with plain and gadolinium-enhanced MR imaging. J Magn Reson Imaging 2000;12:460 – 6. [2] Outwater EK, Dunton CJ. Imaging of the ovary and adnexa: clinical issues and applications of MR imaging. Radiology 1995;194:1 – 18. [3] Hricak H, Stern JL, Fisher MR, Shapeero LG, Winkler ML, Lorey CG. Endometrial carcinoma staging by MR imaging. Radiology 1987;162:297 – 305. [4] Forstner R, Hricak H, White S. CT and MRI of ovarian cancer. Abdom Imaging 1995;20:2 – 8. [5] Worthington JL, Balfe DM, Lee JKT, Gersell DJ, Heiken JP, Ling D, Glazer HS, Jacobs AJ, Kao MS, McClennan BL. Uterine neoplasms: MR imaging. Radiology 1986;159:725 – 30.
152
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
[6] Grasel RP, Outwater EK, Siegelman ES, Capuzzi D, Parker L, Hussain SM. Endometrial polyps: MR imaging features and distinction from endometrial carcinoma. Radiology 2000;214:47 – 52. [7] Imaoka I, Sugimura K, Masui T, Takehara Y, Ichijo K, Naito M. Abnormal uterine cavity: differential diagnosis with MR imaging. Magn Reson Imaging 1999;17:1445 – 55. [8] Sahdev A, Sohaib SA, Jacobs I, Shepherd JH, Oram DH, Reznek RH. MR Imaging of uterine sarcomas. AJR Am J Roentgenol 2001;177: 1307 – 11. [9] Yamashita Y, Takahashi M, Miyazaki K, Okamura H. Contrastenhanced MR imaging of malignant mixed mu¨llerian tumor of the uterus. AJR Am J Roentgenol 1995;160:1150 – 1. [10] Shapeero LG, Hricak H. Mixed mu¨llerian sarcoma of the uterus: MR imaging findings. AJR Am J Roentgenol 1989;153:317 – 9. [11] Koyama T, Togashi K, Konishi I, Kobayashi H, Ueda H, Kataoka ML, Kobayashi H, Itoh T, Higuchi T, Fujii S, Konishi J. MR imaging of endometrial stromal sarcoma: correlation with pathologic findings. AJR Am J Roentgenol 1999;173:767 – 72. [12] Mitchell DG, Mintz MC, Spritzer CE, Gussman D, Arger PH, Coleman BG, Axel L, Kressel HY. Adnexal masses: MR imaging observations at 1.5 T, with US and CT correlation. Radiology 1987; 162:19 – 24. [13] Jain KA, Jeffrey RB. Evaluation of pelvic masses with magnetic resonance imaging and ultrasonography. J Ultrasound Med 1994; 13:845 – 53. [14] Yamashita Y, Torashima M, Hatanaka Y, Harada M, Higashida Y, Takahashi M, Mizutani H, Tashiro H, Iwamasa I, Miyazaki K. Adnexal masses: accuracy of characterization with transvaginal US and
[15]
[16]
[17]
[18]
[19]
[20]
[21]
[22]
precontrast and postcontrast MR imaging. Radiology 1995;194: 557 – 65. Yamaoka T, Togashi K, Koyama T, et al. Yolk sac tumor of the ovary: radiologic – pathologic correlation in four cases. J Comput Assist Tomogr 2000;24:605 – 9. Scoutt LM, McCarthy SM, Lange R, Bourque A, Schwartz PE. MR evaluation of clinically suspected adnexal masses. J Comput Assist Tomogr 1994;18:609 – 18. Medl M, Kulenkampff KJ, Stiskal M, Peters-Engl C, Leodolter S, Czembirek H. Magnetic resonance imaging in the preoperative evaluation of suspected ovarian masses. Anticancer Res 1995;15: 1123 – 6. Togashi K, Nishimura K, Itoh K, Fujisawa I, Sago T, Minami S, Nakano Y, Itoh H, Torizuka K, Ozasa H. Ovarian cystic teratomas: MR imaging. Radiology 1987;162:669 – 73. Morikawa K, Hatabu H, Togashi K, Kataoka ML, Mori T, Konishi I. Granulosa cell tumor of the ovary: MR findings. J Comput Assist Tomogr 1997;21:1001 – 4. Kim SH, Kim WH, Park KJ, Lee JK, Kim JS. CT and MR findings of krukenberg tumors: comparison with primary ovarian tumor. J Comput Assist Tomogr 1996;20:393 – 8. Brown DL, Zou KH, Tempany CMC, Frates MC, Silverman SG, McNeil BJ, Kurtz AB. Primary versus secondary ovarian malignancy: imaging findings of adnexal masses in the radiology diagnostic oncology group study. Radiology 2001;219:213 – 8. Ferrozzi F, Tognini G, Bova D, Zuccoli G. Non-Hodgkin lymphomas of the ovaries: MR findings. J Comput Assist Tomogr 2000;24: 416 – 20.
MRI of gynecological neoplasm Margaret H. Pui a,*, Qiu Yan Wang b, Bin Xu b, Guo Ping Fan b a
Department of Radiology, McMaster University Medical Center, PO Box 2000 Station A, Hamilton, Ontario, Canada L8N 3Z5 b Department of Radiology, Xin Hua Hospital, 1665 Kong Jiang Road, Shanghai, People’s Republic of China Received 1 March 2003; accepted 27 March 2003
Abstract MRI is multiplanar, has large field of view, superior contrast resolution and no known adverse effect on the reproductive potential of ovaries. It is useful for characterizing solid, cystic or necrotic tissue, blood and fat. Contrast-enhanced MRI is also a comprehensive examination of the entire pelvis including lymph nodes, peritoneum, pelvic sidewalls, bone and muscles. It provides information about areas difficult to assess surgically, can refine staging classification, assists in planning surgery or radiotherapy and may be more costeffective by limiting use of surgery. This is a pictorial essay of MRI assessment of female pelvic neoplasm. D 2004 Elsevier Inc. All rights reserved. Index terms: Magnetic resonance imaging; Pelvic tumor; Ovarian tumor; Uterine tumor; Adnexal mass
1. Introduction Transvaginal ultrasound can differentiate between functional cyst, dermoid, some endometriomas, abscess, hydrosalpinx, polycystic ovary and ectopic pregnancy. Because MRI is multiplanar, has large field of view, superior contrast resolution and no known adverse effect on the reproductive potential of ovaries, it is useful for characterizing indeterminate masses. Contrast-enhanced MRI is also a comprehensive examination of the entire pelvis including lymph nodes, peritoneum, pelvic sidewalls, bone and muscles. This is a pictorial essay of MRI assessment of female pelvic neoplasm.
2. Methods Of 140 female patients who underwent MRI investigation of pelvic disease from 1997 through 2001, histological confirmation was obtained in 90 patients (age range: 0.1 –81 years, average: 51.8 years) by surgical excision. Benign lesions included 12 uterine fibroids, 2 cervical polyps, 12 teratomas, 7 cystadenomas, 6 serous cysts, 7
endometriomas of the ovary and 5 pelvic abscesses. The malignant uterine tumors included seven endometrial carcinomas, five cervical carcinomas, one recurrent endometrial stromal sarcoma and one recurrent mixed mu¨llerian tumor. Ovarian malignancy included eight recurrent carcinomas, four serous cystadenocarcinomas, four metastases, three theca cell tumors, one granulosa cell tumor, one yolk sac tumor and one non-Hodgkin’s lymphoma. There were also one each of primary fallopian tube carcinoma and metastases of vagina and peritoneum. In all patients, sagittal, axial and coronal unenhanced turbo spin – echo T2-weighted images (TR/TE/number of acquisitions/echo train length; 3050/150/6/32) and turbo spin – echo T1weighted images (450/10/4/4) before and after intravenous injection of 20 mmol/kg of gadolinium – DTPA were acquired using a 0.5-T MR system. Sixteen images of 6-mm thickness and 0.6-mm interslice gap were obtained with 28 35 cm field of view, 192 256 matrix and acquisition time of 3 min 47 s. The images were reviewed by two radiologists (MHP, QYW) and correlated with histological diagnosis.
3. Discussion * Corresponding author. Tel.: +1-905-521-2100x73200; fax: +1-905522-1390. E-mail address: [email protected] (M.H. Pui). 0899-7071/04/$ – see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/S0899-7071(03)00116-5
MRI has high soft tissue contrast and is useful for characterization of solid, cystic or necrotic tissue, blood
144
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
and fat. It is also helpful for differential diagnosis of endometrial pathology in women who have obliterated cervical canal and unsuccessful dilatation and curettage or endometrial biopsy. MRI provides information about areas difficult to assess surgically including the dome of diaphragm, retroperitoneum and colon. It can refine staging classification and assist in planning surgery or radiotherapy. Exploratory laparotomy has accuracy of 73% compared to 97% accuracy of MRI for assessing depth of myometrial invasion and tumor volume. However,
microscopic peritoneal disease and large pelvic mass distorting anatomic landmark can decrease the staging accuracy to 75% [1 – 4]. Because of the two- to eightfold increased cost of laparoscopy, hysteroscopy, laparotomy and vaginal hysterectomy, and more than half of the suspicious pelvic masses by clinical examination, elevated CA 125 level and ultrasonography are benign, MRI may be more cost-effective by limiting use of surgery. Tumor spill from cyst rupture during laparoscopy or surgery can also be avoided [1,2].
Fig. 1. An 18-year-old girl with ovarian teratoma. (A) Axial T1-, (B) sagittal fat-saturated T2- and (C) sagittal enhanced T1-weighted images show a multilocular complex mass posterior and superior to the normal uterus (arrow). The mass has mixed cystic and solid components with variable signal intensities. The fat content (*) of the tumor immediately posterior to the uterus has high T1 signal and is suppressed on the fat-saturated T2-weighted image. There is moderate contrast enhancement in a portion of the solid tissue posterior to the fat.
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
145
Fig. 2. A 38-year-old woman with multiple large leiomyomas in the posterior uterine wall and fundus extending to the diaphragm. These tumors have welldefined margins with heterogeneous low to intermediate signals on sagittal T2-weighted image (A). The solid tumors (arrow) enhance homogeneously similar to the normal myometrium on the enhanced sagittal T1-weighted image (B). There is central cystic degeneration with T2 hyperintensity and no contrast enhancement.
Normal uterus and ovary have homogeneous intermediate T1 signal intensity on MRI. The uterine corpus has a T2-hyperintense central endometrium, T2-hypointense junctional zone of 3– 10 mm thickness and peripheral myometrium of intermediate T2 signal intensity. The junctional zone is a portion of the myometrium with different blood flow or hydration. The cervix has higher fibrous content with two or three zones of different signal intensities that are lower than the corpus. There is homogeneous contrast enhancement in the endometrium and peripheral myometrium greater than the junctional zone (Fig. 1). Normal ovary has low to intermediate T2 signal with T2-hyperintense follicles in the cortical and subcortical locations [2,5]. Endometrial thickening may represent submucosal leiomyoma, endometrial polyp or hyperplasia, mixed mesenchymal tumor or stromal tumor. Leiomyomas are typically well circumscribed and have low to intermediate T2 signals (Fig. 2). Endometrial polyps are benign nodular protrusions consisting of irregularly distributed endometrial glands, thick-walled blood vessels and dense fibrous or smooth muscle stroma. Polyps have intermediate T1 and heterogeneous high T2 signals. Large polyps distend the endometrial cavity, whereas small polyps blend with the endometrium and are not visible on MRI [6]. Both cases of cervical polyps in our review were not detected on MRI. Adenomatous hyperplasia and hyperplasia with atypia are considered
precancerous. The endometrial thickening is probably benign if high T2 signal and strong contrast enhancement are detected.
Fig. 3. A 66-year-old woman with endometrial carcinoma. Sagittal T2-weighted image demonstrates a 4-cm slightly hyperintense mass (*) in the endometrial cavity invading the junctional zone.
146
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
Fig. 4. Enhanced sagittal T1-weighted image shows mildly enhancing endometrial carcinoma infiltrating the myometrium and posterior bladder wall in a 72-year-old woman.
Fig. 6. A 67-year-old woman with recurrent mixed mu¨llerian tumor. (A) Axial T2-weighted image shows a 10-cm irregular mass with heterogeneous intermediate signal intensity (arrow). There is heterogeneous contrast enhancement of the tumor and ascites on the enhanced sagittal T1-weighted image (B).
Fig. 5. A 46-year-old woman with papillary adenocarcinoma of cervix. (A) Sagittal T2- and (B) enhanced T1-weighted images show a 5-cm cervical mass (arrow) with slightly higher T2 signal than normal myometrium and mild contrast enhancement.
Malignancy is suspected if the endometrial lesion has low to intermediate T2 signal, shows weak contrast enhancement and invades the junctional zone. These criteria have sensitivity of 50 –83%, specificity of 92– 97% and accuracy of 82– 89% for differentiating malignant from benign lesions [7]. Endometrial carcinoma is the most frequent malignant neoplasm of female genital tract (Figs. 3 and 4). It occurs mainly in peri- or postmenopausal women with peak age of 55 – 66 years. Adenocarcinoma accounts for 60 – 70%, adenocanthoma and adenosquamous carcinoma constitute 20– 30%, whereas clear cell, mucinous, secretory and papillary serous carcinomas are uncommon (Fig. 5). Sarcomas constitute 1 –3% of uterine malignancy including mixed mu¨llerian tumor (40 – 70%), leiomyosarcoma (40 – 50%), rhabdomyosarcoma and endometrial stromal sarcoma ( < 10%). Endometrial stromal sarcoma is more common in postmenopausal women with previous pelvic radiotherapy
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
147
Fig. 7. Recurrent endometrial stromal sarcoma in a 69-year-old woman presents as a large lobulated mass (arrow) posterior to the urinary bladder. The tumor has heterogeneous low to intermediate signals on the (A) sagittal T1- and (B) T2-weighted images.
(4– 38%). Clinical presentation of uterine malignancy is late with nonspecific symptoms of vaginal bleeding, pelvic pain or fullness, and sometimes passage of malignant tumor fragments. The sarcomas are heterogeneous masses with low to intermediate T1 and T2 signals and a few pockets of necrosis and bleed with T2 hyperintensities (Figs. 6 and 7). The prognosis and treatment depend on histological grading, nodal metastasis and
extent of myometrial invasion [1]. Mixed mu¨llerian tumors have mixed adenocarcinoma and rhabdomyosarcoma components. Endometrial stromal sarcoma derives from totipotential endometrial stromal cell. Preserved bundles of myometrial fibers are separated by clusters of tumor cells with abundant tumor vessels and prominent involvement of lymphatics and blood vessels. The tumor may be seen as scattered nodules, well-demarcated expansile
Fig. 8. A 52-year-old woman with mucinous cystadenoma of the right ovary. (A) Sagittal T2-weighted image shows a 10-cm septated cystic mass (arrow) with varying fluid signal intensities. The thin septa and cyst wall enhance with contrast on enhanced sagittal T1-weighted image (B).
148
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
Fig. 10. A 15-cm endometrioid adenocarcinoma of the ovary in a 68-yearold woman appears as a solid lobulated mass (arrow) with intermediate T2 signal and small amount of necrosis on (A) sagittal T2-weighted image. (B) Enhanced axial T1-weighted image shows mild homogeneous contrast enhancement and ascites.
Fig. 9. A 44-year-old woman with left ovarian serous papillary cystadenocarcinoma. (A) Axial T1-, (B) T2- and (C) enhanced T1-weighted images show a 9-cm septated cystic mass with multiple enhancing solid mural nodules. The cysts have varying signal intensities caused by hemorrhage and increased protein content.
polypoid mass expanding the endometrial cavity and disrupting the junctional zone, or poorly demarcated diffuse endometrial thickening with irregular junctional zone [8– 11]. Ovarian tumors may arise from surface epithelium (90%), germ cell or stroma. They are often benign (80%) and involve women of reproductive age. Common benign tumors are teratomas, serous and mucinous epithelial tumors. Cystic teratoma consists of cyst lined by epithelium resembling keratinized epidermis with sebaceous and sweat glands, palm-tree-like protrusion and round nodules due to mixture of hair and desquamated epithelial cells. The cyst fluid is rich in protein, has high viscosity and has high T2 signal. Layered debris may be seen due to matted hair with intermediate signal intensity
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
149
Fig. 11. A 60-year-old woman with recurrent clear cell carcinoma of the right ovary and ascites. (A) Axial T1- and (B) T2-weighted images show a 9-cm complex mass (arrowheads) with hemorrhage into both the septated cystic and solid components.
between fat and fluid. MRI has higher accuracy (93%) than ultrasound (86%) in characterizing teratoma (Fig. 1). The fatty content can be detected by chemical shift artifact and fat suppression [2,12 – 15]. Mucinous cystadenomas are multilocular cysts with varying signal intensities, uniform thin septa and wall (Fig. 8). Serous
cystadenomas are unilocular with fluid signal intensity similar to urine. Ovarian malignancy is more common in women older than 45 years of age. Because malignancy presents with minor symptoms of abdominal distention or pressure, 75% of the tumors are Stage II and 60% greater than Stage III
Fig. 12. A 2-month-old infant with a 10-cm yolk sac tumor of the ovary. The tumor displaces the uterus anteriorly (arrow) and has heterogeneous low T1 and high T2 signals on (A) sagittal T1- and (B) T2-weighted images. There is tumor infiltration of the bone marrow with T2 hyperintensity in the L5 vertebra and sacrum relative to the normal L4 vertebral body. The tumor extends to the sacral canal (*).
150
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
germinomas, yolk sac tumors and immature teratomas. Dysgerminomas are solid with hypointense fibrovascular septa and prominent enhancement. Malignant yolk sac tumors are mainly solid with hemorrhage and T2-hyperintense stromal edema (Fig. 12). They are hypervascular with signal voids and enhance more than myometrium [18]. Granulosa cell tumor of the ovary is an estrogen-producing sex and stromal cell tumor. It constitutes less than 10% of ovarian malignancy. It is solid with variable amount of cystic component and blood (Fig. 13). The uterus is enlarged with thick endometrium [19]. Thecoma and fibrothecoma have similar MRI appearance as granulosa cell tumor (Fig. 14). Krukenberg tumors constitute 5 – 10% of ovarian tumors. They commonly result from transcoelomic spread of colonic and gastric carcinoma penetrating the ovary and stimulating dense stromal reaction. Carcinoma of the breast, pancreas, gall bladder, lung and melanoma can
Fig. 13. A 51-year-old woman with granulosa cell tumor. (A) Axial T2- and (B) enhanced T1-weighted images show enlarged left ovary (arrow) with similar T2 signal intensity and contrast enhancement relative to the myometrium. There is central tumor necrosis and thick endometrium (*).
at diagnosis with 5-year survival rates of 80% and 5%, respectively. MRI is 95% sensitive, 89% specific and 96% accurate in differentiating benign from malignant adnexal masses [16]. Criteria for malignancy include large size greater than 4 cm, wall or septal thickness more than 3 mm, nodularity, vegetation or large solid component, necrosis or bleed, rapid and marked contrast enhancement, extension to adjacent organ or sidewall, peritoneal, mesenteric or omental disease, massive ascites and lymphadenopathy [4,16,17]. Epithelial ovarian carcinoma constitutes 85 –90% of all ovarian malignancy and includes serous, mucinous, endometrioid, clear cell and anaplastic carcinomas [2]. Serous papillary carcinoma is the most common and often has papillary projection and cyst content of variable signal intensity (Fig. 9). Endometrioid carcinoma and clear cell carcinoma present as unilocular cysts with nodule (Figs. 10 and 11). Malignant germ cell tumors of the ovary are dys-
Fig. 14. A 66-year-old woman with left ovarian theca cell tumor and ascites. (A) Sagittal T2-weighted image shows tumor mass posterior to the uterus. The tumor has lobulated margins, intermediate T2 signal and small pockets of necrosis. There is less contrast enhancement than the normal myometrium demonstrated on the enhanced axial T1-weighted image (B).
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
151
also metastasize to the ovaries. Ovarian metastases are often bilateral (60 – 80%) and solid (63%) with welldefined margin and preserved ovarian configuration. They have heterogeneous low to intermediate T1 signals. Half of the tumors have low T2 signals and moderate contrast enhancement because of dense collagenous stroma (Fig. 15). Mucin produced by the signet ring cells result in areas of high T2 signal. Ovarian metastases can be detected before the primary tumor is identified [20,21]. Ovarian lymphoma may be a local manifestation of occult lymph nodal disease or secondary site of systemic disease. Non-Hodgkin’s lymphoma accounts for less than 1% of primary ovary malignancy. It presents as a solid mass with homogeneous low to intermediate T1 signal intensity, slightly high T2 signal and mild to moderate contrast enhancement (Fig. 16). It is often bilateral, lobulated
Fig. 16. A 49-year-old woman with non-Hodgkin’s lymphoma of the left ovary. (A) Axial T1- and (B) T2-weighted images show a 3-cm lobular solid mass with homogeneous intermediate signals (arrow). There was mild contrast enhancement and associated left iliac and inguinal lymphadenopathy (not shown).
and associated with generalized lymphadenopathy or multiple lesions in other organs [22].
References
Fig. 15. A 68-year-old woman with ovarian metastases from gastric carcinoma. (A) Axial T2- and (B) enhanced T1-weighted images show a large ovary with preservation of normal ovarian configuration (arrow). The tumor has intermediate T1 and T2 signals and heterogeneous contrast enhancement.
[1] Sacz F, Urresola A, Larena JA, Martin JI, Pijuan JI, Schneider J, Ibanez E. Endometrial carcinoma: assessment of myometrial invasion with plain and gadolinium-enhanced MR imaging. J Magn Reson Imaging 2000;12:460 – 6. [2] Outwater EK, Dunton CJ. Imaging of the ovary and adnexa: clinical issues and applications of MR imaging. Radiology 1995;194:1 – 18. [3] Hricak H, Stern JL, Fisher MR, Shapeero LG, Winkler ML, Lorey CG. Endometrial carcinoma staging by MR imaging. Radiology 1987;162:297 – 305. [4] Forstner R, Hricak H, White S. CT and MRI of ovarian cancer. Abdom Imaging 1995;20:2 – 8. [5] Worthington JL, Balfe DM, Lee JKT, Gersell DJ, Heiken JP, Ling D, Glazer HS, Jacobs AJ, Kao MS, McClennan BL. Uterine neoplasms: MR imaging. Radiology 1986;159:725 – 30.
152
M.H. Pui et al. / Journal of Clinical Imaging 28 (2004) 143–152
[6] Grasel RP, Outwater EK, Siegelman ES, Capuzzi D, Parker L, Hussain SM. Endometrial polyps: MR imaging features and distinction from endometrial carcinoma. Radiology 2000;214:47 – 52. [7] Imaoka I, Sugimura K, Masui T, Takehara Y, Ichijo K, Naito M. Abnormal uterine cavity: differential diagnosis with MR imaging. Magn Reson Imaging 1999;17:1445 – 55. [8] Sahdev A, Sohaib SA, Jacobs I, Shepherd JH, Oram DH, Reznek RH. MR Imaging of uterine sarcomas. AJR Am J Roentgenol 2001;177: 1307 – 11. [9] Yamashita Y, Takahashi M, Miyazaki K, Okamura H. Contrastenhanced MR imaging of malignant mixed mu¨llerian tumor of the uterus. AJR Am J Roentgenol 1995;160:1150 – 1. [10] Shapeero LG, Hricak H. Mixed mu¨llerian sarcoma of the uterus: MR imaging findings. AJR Am J Roentgenol 1989;153:317 – 9. [11] Koyama T, Togashi K, Konishi I, Kobayashi H, Ueda H, Kataoka ML, Kobayashi H, Itoh T, Higuchi T, Fujii S, Konishi J. MR imaging of endometrial stromal sarcoma: correlation with pathologic findings. AJR Am J Roentgenol 1999;173:767 – 72. [12] Mitchell DG, Mintz MC, Spritzer CE, Gussman D, Arger PH, Coleman BG, Axel L, Kressel HY. Adnexal masses: MR imaging observations at 1.5 T, with US and CT correlation. Radiology 1987; 162:19 – 24. [13] Jain KA, Jeffrey RB. Evaluation of pelvic masses with magnetic resonance imaging and ultrasonography. J Ultrasound Med 1994; 13:845 – 53. [14] Yamashita Y, Torashima M, Hatanaka Y, Harada M, Higashida Y, Takahashi M, Mizutani H, Tashiro H, Iwamasa I, Miyazaki K. Adnexal masses: accuracy of characterization with transvaginal US and
[15]
[16]
[17]
[18]
[19]
[20]
[21]
[22]
precontrast and postcontrast MR imaging. Radiology 1995;194: 557 – 65. Yamaoka T, Togashi K, Koyama T, et al. Yolk sac tumor of the ovary: radiologic – pathologic correlation in four cases. J Comput Assist Tomogr 2000;24:605 – 9. Scoutt LM, McCarthy SM, Lange R, Bourque A, Schwartz PE. MR evaluation of clinically suspected adnexal masses. J Comput Assist Tomogr 1994;18:609 – 18. Medl M, Kulenkampff KJ, Stiskal M, Peters-Engl C, Leodolter S, Czembirek H. Magnetic resonance imaging in the preoperative evaluation of suspected ovarian masses. Anticancer Res 1995;15: 1123 – 6. Togashi K, Nishimura K, Itoh K, Fujisawa I, Sago T, Minami S, Nakano Y, Itoh H, Torizuka K, Ozasa H. Ovarian cystic teratomas: MR imaging. Radiology 1987;162:669 – 73. Morikawa K, Hatabu H, Togashi K, Kataoka ML, Mori T, Konishi I. Granulosa cell tumor of the ovary: MR findings. J Comput Assist Tomogr 1997;21:1001 – 4. Kim SH, Kim WH, Park KJ, Lee JK, Kim JS. CT and MR findings of krukenberg tumors: comparison with primary ovarian tumor. J Comput Assist Tomogr 1996;20:393 – 8. Brown DL, Zou KH, Tempany CMC, Frates MC, Silverman SG, McNeil BJ, Kurtz AB. Primary versus secondary ovarian malignancy: imaging findings of adnexal masses in the radiology diagnostic oncology group study. Radiology 2001;219:213 – 8. Ferrozzi F, Tognini G, Bova D, Zuccoli G. Non-Hodgkin lymphomas of the ovaries: MR findings. J Comput Assist Tomogr 2000;24: 416 – 20.