DOI: 10.1148/rg.24si045501
RadioGraphics 2004;24:S147-S166
© RSNA, 2004
LOWER GENITOURINARY TRACT IMAGING |
Functioning Ovarian Tumors: Direct and Indirect Findings at MR Imaging1
Yumiko O. Tanaka, MD,
Hajime Tsunoda, MD,
Yumiko Kitagawa, MD,
Teruko Ueno, MD,
Hiroyuki Yoshikawa, MD and
Yukihisa Saida, MD
1 From the Departments of Radiology (Y.O.T., Y.K., T.U., Y.S.) and Obstetrics and Gynecology (H.T., H.Y.), Graduate School of Comprehensive Human Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575, Japan. Recipient of a Certificate of Merit award for an education exhibit at the 2003 RSNA scientific assembly. Received January 28, 2004; revision requested March 4 and received April 26; accepted May 5. All authors have no financial relationships to disclose. Address correspondence to Y.O.T. (e-mail: ytanaka@md.tsukuba.ac.jp).
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Abstract
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There are many kinds of ovarian tumors and tumorlike conditions that produce estrogen or androgen. Magnetic resonance imaging can demonstrate not only ovarian tumors but also an enlarged uterus with a thick endometrium, even in cases of a clinically latent excess of estrogen. These clinical and indirect imaging findings can aid in the differential diagnosis of ovarian tumors. Granulosa cell tumor and thecoma are well-known estrogen-producing tumors. In pediatric or postmenopausal patients, they manifest as precocious pseudopuberty or postmenopausal bleeding, respectively. Conversely, Sertoli-Leydig cell tumor is representative of hormone-producing tumors that cause virilization. However, there are other functioning ovarian tumors besides the sex cord–stromal tumors. It is well known that metastatic ovarian tumors often have androgen-producing stroma and that mucinous cystadenoma sometimes produces estrogens. Most other ovarian tumors can produce sexual hormones in their stroma. In addition, some endocrinologic abnormalities (eg, polycystic ovary syndrome) also cause virilization.
© RSNA, 2004
Index Terms: Hormones • Ovary, neoplasms, 852.30 • Uterus, abnormalities, 854.30, 854.50
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Introduction
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Many kinds of ovarian tumors produce estrogen or androgen. Sertoli-Leydig cell tumor and steroid cell tumor are examples of androgen-producing tumors that cause virilization. Some tumorlike conditions, such as polycystic ovary syndrome, also cause virilization. Conversely, granulosa cell tumors and thecomas are well-known estrogen-producing tumors. Pediatric or postmenopausal patients with estrogen-producing tumors present with postmenopausal bleeding or isosexual precocity. Magnetic resonance (MR) imaging can demonstrate not only these ovarian tumors directly but also an enlarged uterus with thickened endometrium in such cases. These clinical and indirect imaging findings aid in the differential diagnosis of ovarian tumors. Sex cord–stromal tumors are well-known hormone-producing ovarian tumors; however, other ovarian tumors or tumorlike conditions can also produce sex steroids.
Herein, we discuss the MR imaging characteristics, clinical manifestations, and mechanisms of functional ovarian tumors. Specific topics addressed are synthesis of sex steroids, hyperandrogenism in women, clinical symptoms caused by excess estrogen, morphologic changes in the uterus according to age and intrinsic or exogenous hormones, and ovarian tumors or tumorlike conditions that produce androgens or estrogens.
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Synthesis of Sex Steroids
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Androgens are steroids that stimulate the development of male secondary sex characteristics (Fig 1) and, consequently, promote the growth of sexual hair. The major androgens are dihydrotestosterone, testosterone, dehydroepiandrosterone, dehydroepiandrosterone sulfate, and androstenedione. In nonpregnant women, androgens and their precursors are produced by both the adrenal glands and ovaries in response to their respective tropic hormones, corticotropin and luteinizing hormone. Testosterone is the most important circulating androgen. Approximately half of a woman’s serum testosterone level is derived from peripheral conversion of secreted androstenedione, and the other half is derived from direct glandular secretion. The ovaries and adrenal glands contribute about equally to testosterone production in women (1).
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Figure 1. Synthesis of sex steroids. Androgens are steroids that stimulate the development of male secondary sex characteristics. In nonpregnant women, androgens and their precursors are produced by both the adrenal glands and the ovaries in response to their respective tropic hormones: corticotropin (ACTH) and luteinizing hormone (LH). In the ovaries, androgens are produced as precursors in the synthesis of estrogen and estradiol. The theca cells of preantral (secondary) ovarian follicles produce androstenedione and testosterone in response to luteinizing hormone. In response to follicle-stimulating hormone (FSH), the granulosa cells aromatize these androgens to the estrogens. CRF = corticotropin-releasing factor, LH-RH = luteinizing hormone-releasing hormone.
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Adrenal Production of Androgens
Androgens are produced by the adrenal cortex mainly as intermediates in the formation of cortisol. Consequently, when corticosteroid production is increased, as in Cushing syndrome, the production of androgens may increase and lead to hirsutism or even virilization.
Ovarian Production of Androgens and Estrogens
Androgens are produced by the normal ovaries as precursors in the synthesis of estrogen and estradiol. In response to luteinizing hormone, the theca cells of preantral (secondary) ovarian follicles produce androstenedione and testosterone. In response to follicle-stimulating hormone, the granulosa cells aromatize these androgens to the estrogens.
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Hyperandrogenism in Women
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Gonadal androgens promote midline, facial, and intermammary hair in both men and women. Hirsutism is defined as the presence of hair at androgen-dependent sites where hair does not normally appear in women (Fig 2). This refers particularly to midline hair, sideburns, a mustache, a beard, chest or intermammary hair, inner thigh hair, and midline lower back hair entering the intergluteal area.
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Figure 2. Hyperandrogenism in women. An excess of androgens causes hirsutism and, in severe cases, virilization. Hirsutism involves the presence of hair that does not normally appear in women, such as a mustache. Virilization includes male-pattern baldness, coarsening of the voice, a decrease in breast size, an increase in muscle mass, loss of female body contour, and enlargement of the clitoris.
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Virilization is characterized by male-pattern baldness (located at the vertex most of the time and at the temples occasionally). Coarsening of the voice, a decrease in breast size, an increase in muscle mass, loss of female body contour (obesity, particularly in the upper segment, and change in waist-to-hip ratio), and enlargement of the clitoris also occur.
Virilization is associated with a more severe degree of hyperandrogenism and should raise suspicion of an ovarian or adrenal neoplasm or other hormone-elaborating condition such as polycystic ovary syndrome or Cushing syndrome (2). Differential diagnoses of causes of hyperandrogenism are listed in the Table.
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Clinical Symptoms Caused by Excess Estrogen
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Clinical symptoms caused by excess estrogen vary and are dependent on the patient’s age (Fig 3). As mentioned earlier, estrogen-producing tumors can change the morphologic characteristics of the uterus, especially in the endometrium, where simple hyperplasia usually exhibits some degree of precancerous atypicality (3). The endometrial changes associated with estrogen-producing tumors are manifested clinically in women of reproductive age by metropathia hemorrhagica, which is characterized by irregular and excessive uterine bleeding. Amenorrhea lasting from months to years may precede the abnormal bleeding. Postmenopausal bleeding is the most common endocrine symptom in older women, in whom carcinoma of the endometrium is encountered about twice as often as in younger patients (3).
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Figure 3. Potential effects of excess estrogen. Clinical symptoms caused by excess estrogen vary and are dependent on the patient’s age. Excess estrogen makes the endometrium thicker owing to benign hyperplasia or cancerous proliferation. The myometrium also gets thicker with excess estrogen. These morphologic uterine changes are clinically related to atypical genital bleeding in postmenopausal women and isosexual pseudoprecocity in premenarchal girls. In women of reproductive age, it seldom causes metropathia hemorrhagica.
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Excess of estrogen in premenarchal girls, which is observed in approximately 80% of children with juvenile granulosa cell tumor, results in isosexual precocity. The most common forms of isosexual precocity are those of central origin, with premature release of gonadotropins from the anterior pituitary gland, and those due to apparently autonomous formation of follicular cysts. The precocity caused by granulosa cell tumors is more specifically designated pseudoprecocity because there is no associated ovulation or progesterone production. Typically, pseudoprecocity is heralded by the development of the breasts, followed by the appearance of pubic and axillary hair, stimulation and enlargement of the external and internal secondary sex organs, irregular uterine bleeding, and a whitish vaginal discharge, which is believed to originate from the stimulated endocervical glands. Somatic and skeletal development are typically accelerated as well (4).
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Morphologic Changes in the Uterus according to Age and Intrinsic or Exogenous Hormones
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In women of reproductive age, the uterus is normally 6–9 cm in length and the cervix is narrower and more cylindrical than the corpus (5,6). Within the corpus, three distinct uterine layers can be appreciated: the endometrium, the junctional zone, and the myometrium (6–8). The endometrium is seen as a high-signal-intensity band at the center of the uterus on T2-weighted images. The myometrium has intermediate signal intensity on T2-weighted images, and the junctional zone is seen as an area of low signal intensity at the endometrium-myometrium interface (6–8) (Fig 4a).
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Figure 4a. Sagittal T2-weighted MR images demonstrate uterine morphologic changes according to age and intrinsic or exogenous sex hormones. (a) Image of the uterus obtained during the reproductive period (in a 24-year-old woman) shows that the uterus is 6-9 cm in length and the cervix is smaller than the corpus. There are three zones: an innermost zone of high signal intensity, a middle zone of low signal intensity, and an outermost zone of intermediate signal intensity. These zones correspond to the endometrium, junctional zone, and outer myometrium, respectively. (b, c) MR images of the uterus obtained during childhood (in a 3-year-old girl) (b) and after menopause (in a 65-year-old woman) (c) show that the uterus is small and the zonal anatomy is indistinct (arrows in b). (d) MR image obtained during the reproductive period (in a 34-year-old woman) after the administration of oral contraceptives. The outer myometrium is thicker and brighter, and the junctional zone and the endometrium are thinner. (e) MR image obtained after the administration of a gonadotropin-releasing hormone analogue in a 36-year-old woman with an endometriotic cyst of the ovary (arrow) and adenomyosis. The gonadotropin-releasing hormone analogue caused a hypoestrogenic state and resulted in marked atrophy of the endometrium and an alteration in myometrial signal intensity (arrowheads).
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Figure 4b. Sagittal T2-weighted MR images demonstrate uterine morphologic changes according to age and intrinsic or exogenous sex hormones. (a) Image of the uterus obtained during the reproductive period (in a 24-year-old woman) shows that the uterus is 6-9 cm in length and the cervix is smaller than the corpus. There are three zones: an innermost zone of high signal intensity, a middle zone of low signal intensity, and an outermost zone of intermediate signal intensity. These zones correspond to the endometrium, junctional zone, and outer myometrium, respectively. (b, c) MR images of the uterus obtained during childhood (in a 3-year-old girl) (b) and after menopause (in a 65-year-old woman) (c) show that the uterus is small and the zonal anatomy is indistinct (arrows in b). (d) MR image obtained during the reproductive period (in a 34-year-old woman) after the administration of oral contraceptives. The outer myometrium is thicker and brighter, and the junctional zone and the endometrium are thinner. (e) MR image obtained after the administration of a gonadotropin-releasing hormone analogue in a 36-year-old woman with an endometriotic cyst of the ovary (arrow) and adenomyosis. The gonadotropin-releasing hormone analogue caused a hypoestrogenic state and resulted in marked atrophy of the endometrium and an alteration in myometrial signal intensity (arrowheads).
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Figure 4c. Sagittal T2-weighted MR images demonstrate uterine morphologic changes according to age and intrinsic or exogenous sex hormones. (a) Image of the uterus obtained during the reproductive period (in a 24-year-old woman) shows that the uterus is 6-9 cm in length and the cervix is smaller than the corpus. There are three zones: an innermost zone of high signal intensity, a middle zone of low signal intensity, and an outermost zone of intermediate signal intensity. These zones correspond to the endometrium, junctional zone, and outer myometrium, respectively. (b, c) MR images of the uterus obtained during childhood (in a 3-year-old girl) (b) and after menopause (in a 65-year-old woman) (c) show that the uterus is small and the zonal anatomy is indistinct (arrows in b). (d) MR image obtained during the reproductive period (in a 34-year-old woman) after the administration of oral contraceptives. The outer myometrium is thicker and brighter, and the junctional zone and the endometrium are thinner. (e) MR image obtained after the administration of a gonadotropin-releasing hormone analogue in a 36-year-old woman with an endometriotic cyst of the ovary (arrow) and adenomyosis. The gonadotropin-releasing hormone analogue caused a hypoestrogenic state and resulted in marked atrophy of the endometrium and an alteration in myometrial signal intensity (arrowheads).
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Figure 4d. Sagittal T2-weighted MR images demonstrate uterine morphologic changes according to age and intrinsic or exogenous sex hormones. (a) Image of the uterus obtained during the reproductive period (in a 24-year-old woman) shows that the uterus is 6-9 cm in length and the cervix is smaller than the corpus. There are three zones: an innermost zone of high signal intensity, a middle zone of low signal intensity, and an outermost zone of intermediate signal intensity. These zones correspond to the endometrium, junctional zone, and outer myometrium, respectively. (b, c) MR images of the uterus obtained during childhood (in a 3-year-old girl) (b) and after menopause (in a 65-year-old woman) (c) show that the uterus is small and the zonal anatomy is indistinct (arrows in b). (d) MR image obtained during the reproductive period (in a 34-year-old woman) after the administration of oral contraceptives. The outer myometrium is thicker and brighter, and the junctional zone and the endometrium are thinner. (e) MR image obtained after the administration of a gonadotropin-releasing hormone analogue in a 36-year-old woman with an endometriotic cyst of the ovary (arrow) and adenomyosis. The gonadotropin-releasing hormone analogue caused a hypoestrogenic state and resulted in marked atrophy of the endometrium and an alteration in myometrial signal intensity (arrowheads).
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Figure 4e. Sagittal T2-weighted MR images demonstrate uterine morphologic changes according to age and intrinsic or exogenous sex hormones. (a) Image of the uterus obtained during the reproductive period (in a 24-year-old woman) shows that the uterus is 6-9 cm in length and the cervix is smaller than the corpus. There are three zones: an innermost zone of high signal intensity, a middle zone of low signal intensity, and an outermost zone of intermediate signal intensity. These zones correspond to the endometrium, junctional zone, and outer myometrium, respectively. (b, c) MR images of the uterus obtained during childhood (in a 3-year-old girl) (b) and after menopause (in a 65-year-old woman) (c) show that the uterus is small and the zonal anatomy is indistinct (arrows in b). (d) MR image obtained during the reproductive period (in a 34-year-old woman) after the administration of oral contraceptives. The outer myometrium is thicker and brighter, and the junctional zone and the endometrium are thinner. (e) MR image obtained after the administration of a gonadotropin-releasing hormone analogue in a 36-year-old woman with an endometriotic cyst of the ovary (arrow) and adenomyosis. The gonadotropin-releasing hormone analogue caused a hypoestrogenic state and resulted in marked atrophy of the endometrium and an alteration in myometrial signal intensity (arrowheads).
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Uterine volume and the width of each layer vary throughout the menstrual cycle and with age. In the premenarchal girl, the corpus is small and the cervix is longer than the body of the uterus (and continues to account for more than half of the uterine length until approximately the 13th year) (5) (Fig 4b). The endometrium is thin or not visible, the junctional zone is indistinct, and the myometrium has a lower signal intensity than that in postmenarchal women. In postmenopausal women, the zonal anatomy is indistinct, the endometrium is less than 5 mm thick, and the myometrium has a lower signal intensity than that in premenopausal women (7) (Fig 4c).
Exogenous hormone therapy also changes the morphologic characteristics of the uterus. With oral contraceptive use, the widths of the endometrium and the junctional zone become smaller and the myometrium becomes relatively brighter on T2-weighted images (8) (Fig 4d). Gonadotropin-releasing hormone analogue causes a hypoestrogenic state, and it results in marked atrophy of the endometrium and an alteration in myometrial signal intensity similar to that seen in postmenopausal women (5) (Fig 4e). In patients undergoing estrogen replacement therapy, the appearance of the uterus is similar to that of a woman of reproductive age. Estrogen-producing ovarian tumors also change the morphologic characteristics of the uterus to those of a woman of reproductive age and cause varying symptoms related to the enlarged uterus, especially thickened endometrium. Ovarian tumors and tumorlike conditions that can produce estrogen are also listed in the Table (9).
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Ovarian Tumors or Tumorlike Conditions That Produce Androgens or Estrogens
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Sertoli-Leydig Cell Tumors
Sertoli stromal tumors (androblastomas) are one of the categories of sex cord–stromal tumors of the ovary. They contain Sertoli cells, Leydig cells, fibroblasts, or a combination of these cells. They are composed of Sertoli cell tumors, Leydig cell tumors, and Sertoli-Leydig cell tumors. Sertoli cell tumors account for only 4% of those tumors and are usually nonfunctioning. Leydig cell tumors are classified as steroid cell tumors (discussed later).
Sertoli-Leydig cell tumors are divided into four subtypes: well differentiated, intermediately differentiated, poorly differentiated, and retiform. Three of these subtypes have variants that contain heterologous elements. Seventy-five percent of patients with Sertoli-Leydig tumors are 30 years of age or younger (mean age, 25 years). Virilization occurs in only about one-third of patients. Although these tumors vary in gross appearance, they rarely contain cysts. Tumors with retiform or heterologous components are more often cystic. Most of these tumors are unilateral, and 80% are diagnosed as stage I disease (10). According to reported imaging findings of Sertoli-Leydig cell tumors, they usually appear as solid masses and their signal intensity at T2-weighted imaging is not as low as expected, although they do contain fibrous stroma (11,12) (Fig 5). Sertoli-Leydig cell tumors in patients with virilization are often small and difficult to detect, even with transvaginal ultrasonography (13).
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Figure 5a. Retiform Sertoli-Leydig cell tumor of intermediate differentiation in a 32-year-old pregnant woman. (a) Axial T2-weighted MR image shows a large, lobulated, solid mass (arrowheads) with peripheral cysts (arrow). (b) Axial T1-weighted MR image shows that the contents of the cyst have slightly high signal intensity (arrow). Ut = uterus. Because the patient’s pregnancy was in the 12th gestational week, contrast material was not administered. The surgical specimen obtained at left salpingo-oophorectomy revealed a lobulated mass with rich solid components. (c) High-power photomicrograph (hematoxylin-eosin [H-E] stain) shows that thin cords of darkly staining Sertoli cells lie in the edematous stroma. The pathologic diagnosis was a Sertoli-Leydig cell tumor of intermediate differentiation with a retiform component. Although Sertoli-Leydig cell tumors are reported as predominantly solid masses, cyst formation is common in retiform subtypes and those with heterologous elements. The patient did not show any virilization; however, the serum level of inhibin A was elevated (190.2 pg/mL; normal level, <150 pg/mL), a finding that is another marker of a sex steroid-producing tumor.
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Figure 5b. Retiform Sertoli-Leydig cell tumor of intermediate differentiation in a 32-year-old pregnant woman. (a) Axial T2-weighted MR image shows a large, lobulated, solid mass (arrowheads) with peripheral cysts (arrow). (b) Axial T1-weighted MR image shows that the contents of the cyst have slightly high signal intensity (arrow). Ut = uterus. Because the patient’s pregnancy was in the 12th gestational week, contrast material was not administered. The surgical specimen obtained at left salpingo-oophorectomy revealed a lobulated mass with rich solid components. (c) High-power photomicrograph (hematoxylin-eosin [H-E] stain) shows that thin cords of darkly staining Sertoli cells lie in the edematous stroma. The pathologic diagnosis was a Sertoli-Leydig cell tumor of intermediate differentiation with a retiform component. Although Sertoli-Leydig cell tumors are reported as predominantly solid masses, cyst formation is common in retiform subtypes and those with heterologous elements. The patient did not show any virilization; however, the serum level of inhibin A was elevated (190.2 pg/mL; normal level, <150 pg/mL), a finding that is another marker of a sex steroid-producing tumor.
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Figure 5c. Retiform Sertoli-Leydig cell tumor of intermediate differentiation in a 32-year-old pregnant woman. (a) Axial T2-weighted MR image shows a large, lobulated, solid mass (arrowheads) with peripheral cysts (arrow). (b) Axial T1-weighted MR image shows that the contents of the cyst have slightly high signal intensity (arrow). Ut = uterus. Because the patient’s pregnancy was in the 12th gestational week, contrast material was not administered. The surgical specimen obtained at left salpingo-oophorectomy revealed a lobulated mass with rich solid components. (c) High-power photomicrograph (hematoxylin-eosin [H-E] stain) shows that thin cords of darkly staining Sertoli cells lie in the edematous stroma. The pathologic diagnosis was a Sertoli-Leydig cell tumor of intermediate differentiation with a retiform component. Although Sertoli-Leydig cell tumors are reported as predominantly solid masses, cyst formation is common in retiform subtypes and those with heterologous elements. The patient did not show any virilization; however, the serum level of inhibin A was elevated (190.2 pg/mL; normal level, <150 pg/mL), a finding that is another marker of a sex steroid-producing tumor.
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Steroid Cell Tumors
Steroid cell tumors are defined as ovarian neoplasms composed entirely of cells resembling typical steroid hormone–secreting cells, that is, lutein cells, Leydig cells, and adrenocortical cells. Stromal luteoma, Leydig cell tumor, and steroid cell tumor not otherwise specified are included in this group; all of these tumor types are very rare (14). Some tumors in the last category are clinically malignant, whereas those in the first two categories are benign (14). At gross examination, stromal luteomas are well-circumscribed solid tumors within the ovary. They are difficult to identify because they are almost always smaller than 3 cm in diameter. Leydig cell tumors are reported to have low attenuation at computed tomography owing to the abundance of lipids in the cytoplasm. None of these have high signal intensity on T1-weighted MR images (15,16). Signal intensities on T2-weighted images vary according to the contents of the fibrous stroma (11,15,16). A steroid cell tumor not otherwise specified is reported as a solid lobulated mass with a few small cysts. The tumor has intermediate signal intensity on T2-weighted images and enhances intensely with contrast material (17).
Granulosa Cell Tumors
Granulosa cell tumor (GCT) is the most common ovarian tumor with estrogenic manifestations that is classified as a sex cord–stromal tumor. Two main pathologic subtypes exist: adult and juvenile. These subtypes are defined by means of histopathologic findings, although the juvenile form affects prepubertal children. As mentioned earlier, GCTs cause pseudoprecocity.
At gross examination, juvenile GCT is a solid and cystic neoplasm, in which the cyst may contain hemorrhagic fluid. Microscopic examination typically reveals a solid cellular neoplasm with focal follicle formation. To our knowledge, only two single case reports have been published, in which juvenile GCT appeared as a large, multicystic mass with heterogeneous enhancement of the solid components (18,19). In our experience, we observed a juvenile GCT that was an entirely solid mass with high signal intensity at T2-weighted imaging and homogeneous contrast enhancement (Fig 6), since there were not many follicles in the tumor.
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Figure 6a. Juvenile GCT in a 2-year-old girl who showed development of the breasts, the appearance of pubic hair, and atypical genital bleeding. (a) Sagittal T2-weighted MR image demonstrates a large solid mass with high signal intensity (arrows) and an enlarged uterus with thick endometrium (arrowheads). Ascites is also seen. (b) Sagittal contrast material-enhanced T1-weighted MR image shows that the tumor (arrows) is homogeneously enhanced. (c) Photomicrograph (original magnification, x10; H-E stain) shows that the tumor cells have abundant eosinophilic cytoplasm and round nuclei and are growing in solid nodules. The patient’s elevated serum estradiol level (33.7 pg/mL [123.7 pmol/L]) decreased (<10 pg/mL [36.7 pmol/L]) immediately after right salpingo-oophorectomy.
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Figure 6b. Juvenile GCT in a 2-year-old girl who showed development of the breasts, the appearance of pubic hair, and atypical genital bleeding. (a) Sagittal T2-weighted MR image demonstrates a large solid mass with high signal intensity (arrows) and an enlarged uterus with thick endometrium (arrowheads). Ascites is also seen. (b) Sagittal contrast material-enhanced T1-weighted MR image shows that the tumor (arrows) is homogeneously enhanced. (c) Photomicrograph (original magnification, x10; H-E stain) shows that the tumor cells have abundant eosinophilic cytoplasm and round nuclei and are growing in solid nodules. The patient’s elevated serum estradiol level (33.7 pg/mL [123.7 pmol/L]) decreased (<10 pg/mL [36.7 pmol/L]) immediately after right salpingo-oophorectomy.
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Figure 6c. Juvenile GCT in a 2-year-old girl who showed development of the breasts, the appearance of pubic hair, and atypical genital bleeding. (a) Sagittal T2-weighted MR image demonstrates a large solid mass with high signal intensity (arrows) and an enlarged uterus with thick endometrium (arrowheads). Ascites is also seen. (b) Sagittal contrast material-enhanced T1-weighted MR image shows that the tumor (arrows) is homogeneously enhanced. (c) Photomicrograph (original magnification, x10; H-E stain) shows that the tumor cells have abundant eosinophilic cytoplasm and round nuclei and are growing in solid nodules. The patient’s elevated serum estradiol level (33.7 pg/mL [123.7 pmol/L]) decreased (<10 pg/mL [36.7 pmol/L]) immediately after right salpingo-oophorectomy.
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Adult GCTs often occur in peri- and postmenopausal women and result in endometrial hyperplasia and atypical genital bleeding. At gross examination, the most characteristic finding is a predominantly cystic tumor that has numerous compartments filled with clotted blood and separated by solid tissue. Adult GCTs, however, grow in a wide variety of patterns, including microfollicular, macrofollicular, insular, trabecular, solid-tubular, and holly-tubular patterns. The typical MR imaging finding is a spongelike, multilocular cystic mass filled with some blood clots (20) (Fig 7), although MR imaging findings of adult GCTs vary from entirely cystic to entirely solid according to histologic variations (21,22).
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Figure 7a. Adult GCT in a 68-year-old woman. (a, b) Axial T2-weighted (a) and sagittal T1-weighted (b) MR images demonstrate a multilocular cystic mass (arrows) with relatively thick septa. The septa have low signal intensity on the T2-weighted image (a). The signal intensity of the fluid within the cysts is very high on the T1-weighted image (b), a finding indicative of hemorrhagic contents. Compared with those seen in healthy postmenopausal women, the uterus is bigger and the endometrium is brighter on the T2-weighted image (arrowheads in a). (c) Sagittal contrast-enhanced T1-weighted MR image obtained with fat saturation shows that the septa have intense enhancement (arrows). A multilocular hemorrhagic mass was removed. (d) High-power photomicrograph (H-E stain) shows cells with oval and angular nuclei and scanty cytoplasm proliferating in trabeculae and cords separated by fibrous tissue. Some red blood cells are also seen, a finding that corresponds to the hypervascular nature evident at imaging. This case demonstrates the most common imaging appearance of GCT—a microfollicular pattern. The elevated serum estradiol level (69.6 pg/mL [255.4 pmol/L]) returned to normal (<8 pg/mL [29.4 pmol/L]) after surgery.
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Figure 7b. Adult GCT in a 68-year-old woman. (a, b) Axial T2-weighted (a) and sagittal T1-weighted (b) MR images demonstrate a multilocular cystic mass (arrows) with relatively thick septa. The septa have low signal intensity on the T2-weighted image (a). The signal intensity of the fluid within the cysts is very high on the T1-weighted image (b), a finding indicative of hemorrhagic contents. Compared with those seen in healthy postmenopausal women, the uterus is bigger and the endometrium is brighter on the T2-weighted image (arrowheads in a). (c) Sagittal contrast-enhanced T1-weighted MR image obtained with fat saturation shows that the septa have intense enhancement (arrows). A multilocular hemorrhagic mass was removed. (d) High-power photomicrograph (H-E stain) shows cells with oval and angular nuclei and scanty cytoplasm proliferating in trabeculae and cords separated by fibrous tissue. Some red blood cells are also seen, a finding that corresponds to the hypervascular nature evident at imaging. This case demonstrates the most common imaging appearance of GCT—a microfollicular pattern. The elevated serum estradiol level (69.6 pg/mL [255.4 pmol/L]) returned to normal (<8 pg/mL [29.4 pmol/L]) after surgery.
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Figure 7c. Adult GCT in a 68-year-old woman. (a, b) Axial T2-weighted (a) and sagittal T1-weighted (b) MR images demonstrate a multilocular cystic mass (arrows) with relatively thick septa. The septa have low signal intensity on the T2-weighted image (a). The signal intensity of the fluid within the cysts is very high on the T1-weighted image (b), a finding indicative of hemorrhagic contents. Compared with those seen in healthy postmenopausal women, the uterus is bigger and the endometrium is brighter on the T2-weighted image (arrowheads in a). (c) Sagittal contrast-enhanced T1-weighted MR image obtained with fat saturation shows that the septa have intense enhancement (arrows). A multilocular hemorrhagic mass was removed. (d) High-power photomicrograph (H-E stain) shows cells with oval and angular nuclei and scanty cytoplasm proliferating in trabeculae and cords separated by fibrous tissue. Some red blood cells are also seen, a finding that corresponds to the hypervascular nature evident at imaging. This case demonstrates the most common imaging appearance of GCT—a microfollicular pattern. The elevated serum estradiol level (69.6 pg/mL [255.4 pmol/L]) returned to normal (<8 pg/mL [29.4 pmol/L]) after surgery.
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Figure 7d. Adult GCT in a 68-year-old woman. (a, b) Axial T2-weighted (a) and sagittal T1-weighted (b) MR images demonstrate a multilocular cystic mass (arrows) with relatively thick septa. The septa have low signal intensity on the T2-weighted image (a). The signal intensity of the fluid within the cysts is very high on the T1-weighted image (b), a finding indicative of hemorrhagic contents. Compared with those seen in healthy postmenopausal women, the uterus is bigger and the endometrium is brighter on the T2-weighted image (arrowheads in a). (c) Sagittal contrast-enhanced T1-weighted MR image obtained with fat saturation shows that the septa have intense enhancement (arrows). A multilocular hemorrhagic mass was removed. (d) High-power photomicrograph (H-E stain) shows cells with oval and angular nuclei and scanty cytoplasm proliferating in trabeculae and cords separated by fibrous tissue. Some red blood cells are also seen, a finding that corresponds to the hypervascular nature evident at imaging. This case demonstrates the most common imaging appearance of GCT—a microfollicular pattern. The elevated serum estradiol level (69.6 pg/mL [255.4 pmol/L]) returned to normal (<8 pg/mL [29.4 pmol/L]) after surgery.
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Although juvenile GCTs tend to be less well differentiated than the adult type at microscopic examination, the prognosis of patients with juvenile GCTs is excellent because most juvenile GCTs represent stage I disease. Conversely, adult GCTs of all patterns have a malignant potential, and late recurrence even 3 or more decades after surgery is not uncommon (23).
Thecoma
Thecoma is also a kind of sex cord–stromal tumor and can be divided into typical and luteinized subtypes. The thecoma occurs at an older average age than does the GCT, and more than 80% of patients are postmenopausal. Sixty percent of postmenopausal patients present with uterine bleeding, and more than 20% have endometrial carcinoma. At gross examination, thecomas appear as solid masses of varying sizes, occasionally with cystic changes. The typical thecoma is composed of swollen lipid-laden stromal cells that resemble theca cells; varying numbers of fibroblasts are usually present as well. Thecomas containing steroid-type cells resembling luteinized theca and luteinized stromal cells are called luteinized thecoma. Luteinized thecoma occurs in a younger age group than does typical thecoma. Half of luteinized thecomas are estrogenic, 39% are nonfunctioning, and 11% are androgenic (24) (Fig 8).
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Figure 8a. Thecoma in a 17-year-old girl with marked virilization and primary amenorrhea. (a) Axial T2-weighted MR image shows a mixed solid and cystic left ovarian mass; the solid part has marked low signal intensity (arrowheads). (b) Axial T1-weighted MR images obtained before (left) and 120 seconds after (right) contrast material administration show a multilocular cystic component on the ventral side of the tumor; the cystic component is filled with high-signal-intensity fluid (arrow). The solid part of the mass is intensely enhanced during the early phase of the dynamic contrast material study (right). (c) Sagittal T2-weighted MR image shows an atrophic uterus (arrows). The patient also had hirsutism, a hypertrophic clitoris, mild obesity, and deepening of the voice. (d) High-power photomicrograph (H-E stain) of a specimen from the yellowish, predominantly solid tumor removed from the patient. The tumor is composed of oval or round tumor cells and has abundant pale cytoplasm containing lipid within a fibromatous background. The elevated serum testosterone level (113.9 ng/dL [4.0 nmol/L]; normal range, 6-86 ng/dL [0.2-3.0 nmol/L]) decreased immediately after surgery (29.6 ng/dL [1.0 nmol/L]).
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Figure 8b. Thecoma in a 17-year-old girl with marked virilization and primary amenorrhea. (a) Axial T2-weighted MR image shows a mixed solid and cystic left ovarian mass; the solid part has marked low signal intensity (arrowheads). (b) Axial T1-weighted MR images obtained before (left) and 120 seconds after (right) contrast material administration show a multilocular cystic component on the ventral side of the tumor; the cystic component is filled with high-signal-intensity fluid (arrow). The solid part of the mass is intensely enhanced during the early phase of the dynamic contrast material study (right). (c) Sagittal T2-weighted MR image shows an atrophic uterus (arrows). The patient also had hirsutism, a hypertrophic clitoris, mild obesity, and deepening of the voice. (d) High-power photomicrograph (H-E stain) of a specimen from the yellowish, predominantly solid tumor removed from the patient. The tumor is composed of oval or round tumor cells and has abundant pale cytoplasm containing lipid within a fibromatous background. The elevated serum testosterone level (113.9 ng/dL [4.0 nmol/L]; normal range, 6-86 ng/dL [0.2-3.0 nmol/L]) decreased immediately after surgery (29.6 ng/dL [1.0 nmol/L]).
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Figure 8c. Thecoma in a 17-year-old girl with marked virilization and primary amenorrhea. (a) Axial T2-weighted MR image shows a mixed solid and cystic left ovarian mass; the solid part has marked low signal intensity (arrowheads). (b) Axial T1-weighted MR images obtained before (left) and 120 seconds after (right) contrast material administration show a multilocular cystic component on the ventral side of the tumor; the cystic component is filled with high-signal-intensity fluid (arrow). The solid part of the mass is intensely enhanced during the early phase of the dynamic contrast material study (right). (c) Sagittal T2-weighted MR image shows an atrophic uterus (arrows). The patient also had hirsutism, a hypertrophic clitoris, mild obesity, and deepening of the voice. (d) High-power photomicrograph (H-E stain) of a specimen from the yellowish, predominantly solid tumor removed from the patient. The tumor is composed of oval or round tumor cells and has abundant pale cytoplasm containing lipid within a fibromatous background. The elevated serum testosterone level (113.9 ng/dL [4.0 nmol/L]; normal range, 6-86 ng/dL [0.2-3.0 nmol/L]) decreased immediately after surgery (29.6 ng/dL [1.0 nmol/L]).
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Figure 8d. Thecoma in a 17-year-old girl with marked virilization and primary amenorrhea. (a) Axial T2-weighted MR image shows a mixed solid and cystic left ovarian mass; the solid part has marked low signal intensity (arrowheads). (b) Axial T1-weighted MR images obtained before (left) and 120 seconds after (right) contrast material administration show a multilocular cystic component on the ventral side of the tumor; the cystic component is filled with high-signal-intensity fluid (arrow). The solid part of the mass is intensely enhanced during the early phase of the dynamic contrast material study (right). (c) Sagittal T2-weighted MR image shows an atrophic uterus (arrows). The patient also had hirsutism, a hypertrophic clitoris, mild obesity, and deepening of the voice. (d) High-power photomicrograph (H-E stain) of a specimen from the yellowish, predominantly solid tumor removed from the patient. The tumor is composed of oval or round tumor cells and has abundant pale cytoplasm containing lipid within a fibromatous background. The elevated serum testosterone level (113.9 ng/dL [4.0 nmol/L]; normal range, 6-86 ng/dL [0.2-3.0 nmol/L]) decreased immediately after surgery (29.6 ng/dL [1.0 nmol/L]).
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Most thecomas appear as admixtures of fibroma and thecoma components, so-called fibrothecoma. Smaller fibrothecomas have homogeneous low signal intensity on both T1- and T2-weighted images, which reflects the abundant fibrous tissue (25–28). At T2-weighted imaging, however, large fibrothecomas have varying amounts of high-signal-intensity areas, which are caused by edema and cystic degeneration (26). Theca cells in the normal ovary are highly vascularized, whereas fibrous tissue is known for delayed weak enhancement at dynamic contrast-enhanced imaging. Therefore, the degree of contrast enhancement varies with the amount of fibrous tissue in the thecoma (29) (Fig 9).
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Figure 9a. Fibrothecoma in a 60-year-old woman. (a) Sagittal T2-weighted MR image shows a large, lobulated, entirely solid tumor (arrows). Although a supravaginal resection had been performed before the MR imaging examination, the remaining portion of the uterus is enlarged and cervical glands (arrowheads) show very high signal intensity. (b) Sagittal contrast-enhanced T1-weighted MR image shows that only the peripheral portion of the tumor (arrows) is weakly enhanced. A solid yellow mass was removed. (c) Low-power photomicrograph obtained with fat stain (oil red-O stain) reveals that the tumor cells contain abundant intracytoplasmic lipid within fibromatous tissue. (Reprinted, with permission, from reference 30.)
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Figure 9b. Fibrothecoma in a 60-year-old woman. (a) Sagittal T2-weighted MR image shows a large, lobulated, entirely solid tumor (arrows). Although a supravaginal resection had been performed before the MR imaging examination, the remaining portion of the uterus is enlarged and cervical glands (arrowheads) show very high signal intensity. (b) Sagittal contrast-enhanced T1-weighted MR image shows that only the peripheral portion of the tumor (arrows) is weakly enhanced. A solid yellow mass was removed. (c) Low-power photomicrograph obtained with fat stain (oil red-O stain) reveals that the tumor cells contain abundant intracytoplasmic lipid within fibromatous tissue. (Reprinted, with permission, from reference 30.)
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Figure 9c. Fibrothecoma in a 60-year-old woman. (a) Sagittal T2-weighted MR image shows a large, lobulated, entirely solid tumor (arrows). Although a supravaginal resection had been performed before the MR imaging examination, the remaining portion of the uterus is enlarged and cervical glands (arrowheads) show very high signal intensity. (b) Sagittal contrast-enhanced T1-weighted MR image shows that only the peripheral portion of the tumor (arrows) is weakly enhanced. A solid yellow mass was removed. (c) Low-power photomicrograph obtained with fat stain (oil red-O stain) reveals that the tumor cells contain abundant intracytoplasmic lipid within fibromatous tissue. (Reprinted, with permission, from reference 30.)
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Sclerosing Stromal Tumor
Sclerosing stromal tumor is one of the benign sex cord–stromal tumors that affect women younger than 30 years of age. This tumor often manifests as menstrual irregularity, although a few cases have androgenic or estrogenic manifestations. At microscopic examination, this tumor is characterized by a pseudolobular pattern, in which cellular areas are separated by edematous and collagenous hypocellular tissue. Pseudolobulation is demonstrated as an admixture of low-signal-intensity nodules set against the high-signal-intensity stroma on T2-weighted images (31). This tumor is also known as a hypervascular tumor and shows early peripheral enhancement with centripetal progression (32–34) (Fig 10).
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Figure 10a. Sclerosing stromal tumor in a 32-year-old woman. Sagittal T2- and T1-weighted MR images show that there is a huge, predominantly solid mass in front of the uterus. (a) T2-weighted image shows that the mass is composed of an admixture of low-signal-intensity nodules (arrows) set against the high-signal-intensity stroma. (b) Contrast-enhanced T1-weighted image shows that the nodules (arrows) enhance more than the stroma. The resected specimen was a huge, yellowish, solid tumor with edematous change and weighed 1,550 g. (c) Loupe image of the specimen (H-E stain) shows a pseudolobular pattern, in which cellular pseudolobules are separated by edematous hypocellular fibrous tissue. The finding of low-signal-intensity nodules within the high-signal-intensity stroma at T2-weighted imaging corresponds to the pseudolobular pattern. The cellular components of the nodules consist of a disorganized admixture of fibroblasts and rounded, vacuolated cells.
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Figure 10b. Sclerosing stromal tumor in a 32-year-old woman. Sagittal T2- and T1-weighted MR images show that there is a huge, predominantly solid mass in front of the uterus. (a) T2-weighted image shows that the mass is composed of an admixture of low-signal-intensity nodules (arrows) set against the high-signal-intensity stroma. (b) Contrast-enhanced T1-weighted image shows that the nodules (arrows) enhance more than the stroma. The resected specimen was a huge, yellowish, solid tumor with edematous change and weighed 1,550 g. (c) Loupe image of the specimen (H-E stain) shows a pseudolobular pattern, in which cellular pseudolobules are separated by edematous hypocellular fibrous tissue. The finding of low-signal-intensity nodules within the high-signal-intensity stroma at T2-weighted imaging corresponds to the pseudolobular pattern. The cellular components of the nodules consist of a disorganized admixture of fibroblasts and rounded, vacuolated cells.
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Figure 10c. Sclerosing stromal tumor in a 32-year-old woman. Sagittal T2- and T1-weighted MR images show that there is a huge, predominantly solid mass in front of the uterus. (a) T2-weighted image shows that the mass is composed of an admixture of low-signal-intensity nodules (arrows) set against the high-signal-intensity stroma. (b) Contrast-enhanced T1-weighted image shows that the nodules (arrows) enhance more than the stroma. The resected specimen was a huge, yellowish, solid tumor with edematous change and weighed 1,550 g. (c) Loupe image of the specimen (H-E stain) shows a pseudolobular pattern, in which cellular pseudolobules are separated by edematous hypocellular fibrous tissue. The finding of low-signal-intensity nodules within the high-signal-intensity stroma at T2-weighted imaging corresponds to the pseudolobular pattern. The cellular components of the nodules consist of a disorganized admixture of fibroblasts and rounded, vacuolated cells.
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Ovarian Tumors with Functioning Stroma
Because of their hormonal activity, the stromal cells of ovarian tumors have attracted the attention of gynecologic pathologists. Various ovarian tumors with both estrogenic and androgenic manifestations have been reported (35). Results of laboratory studies have shown that surface epithelial tumors, especially mucinous cystadenomas, are the most common type to have an estrogenic stroma. Conversely, among the more than 60 reported ovarian tumors with an androgenic stroma, one-third are metastatic ovarian tumors, mostly of gastric origin, and one-fifth are primary mucinous cystic tumors. Brenner tumors, teratomas, and carcinoids can also have androgen-producing stroma (35,36) (Fig 11).
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Figure 11a. Ovarian carcinoid with testosterone-producing stroma in a 54-year-old woman. (a) Sagittal T2-weighted MR image shows a multilocular cystic mass with fluid of varying signal intensities in the lower abdomen. The mass contains a relatively large mural nodule (arrows), which has low signal intensity. (b) Sagittal contrast-enhanced T1-weighted MR image shows that the nodule has homogeneous enhancement (arrows). The patient had hirsutism and slight clitoromegaly. Laboratory data showed increased concentrations of serum testosterone (371.2 ng/dL [12.9 nmol/L]). Therefore, the preoperative radiologic diagnosis was a Sertoli-Leydig cell tumor. The cut surface of the resected specimen showed a multilocular cystic mass with a large white mural nodule. (c) Low-power photomicrograph (H-E stain) reveals medium-sized tumor cells proliferating in a solid and insular pattern accompanied by a delicate fibrous stroma. The tumor was positive for neuroendocrine markers at immunohistochemical staining, which helped determine the diagnosis of ovarian carcinoid. (d) High-power photomicrograph shows that the stroma is also positive for  -inhibin stain (arrows), a finding that indicates that the stroma produces androgen. The serum testosterone level returned to normal after surgery (8.2 ng/dL [0.3 nmol/L]). (Reprinted, with permission, from reference 36.)
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Figure 11b. Ovarian carcinoid with testosterone-producing stroma in a 54-year-old woman. (a) Sagittal T2-weighted MR image shows a multilocular cystic mass with fluid of varying signal intensities in the lower abdomen. The mass contains a relatively large mural nodule (arrows), which has low signal intensity. (b) Sagittal contrast-enhanced T1-weighted MR image shows that the nodule has homogeneous enhancement (arrows). The patient had hirsutism and slight clitoromegaly. Laboratory data showed increased concentrations of serum testosterone (371.2 ng/dL [12.9 nmol/L]). Therefore, the preoperative radiologic diagnosis was a Sertoli-Leydig cell tumor. The cut surface of the resected specimen showed a multilocular cystic mass with a large white mural nodule. (c) Low-power photomicrograph (H-E stain) reveals medium-sized tumor cells proliferating in a solid and insular pattern accompanied by a delicate fibrous stroma. The tumor was positive for neuroendocrine markers at immunohistochemical staining, which helped determine the diagnosis of ovarian carcinoid. (d) High-power photomicrograph shows that the stroma is also positive for -inhibin stain (arrows), a finding that indicates that the stroma produces androgen. The serum testosterone level returned to normal after surgery (8.2 ng/dL [0.3 nmol/L]). (Reprinted, with permission, from reference 36.)
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Figure 11c. Ovarian carcinoid with testosterone-producing stroma in a 54-year-old woman. (a) Sagittal T2-weighted MR image shows a multilocular cystic mass with fluid of varying signal intensities in the lower abdomen. The mass contains a relatively large mural nodule (arrows), which has low signal intensity. (b) Sagittal contrast-enhanced T1-weighted MR image shows that the nodule has homogeneous enhancement (arrows). The patient had hirsutism and slight clitoromegaly. Laboratory data showed increased concentrations of serum testosterone (371.2 ng/dL [12.9 nmol/L]). Therefore, the preoperative radiologic diagnosis was a Sertoli-Leydig cell tumor. The cut surface of the resected specimen showed a multilocular cystic mass with a large white mural nodule. (c) Low-power photomicrograph (H-E stain) reveals medium-sized tumor cells proliferating in a solid and insular pattern accompanied by a delicate fibrous stroma. The tumor was positive for neuroendocrine markers at immunohistochemical staining, which helped determine the diagnosis of ovarian carcinoid. (d) High-power photomicrograph shows that the stroma is also positive for -inhibin stain (arrows), a finding that indicates that the stroma produces androgen. The serum testosterone level returned to normal after surgery (8.2 ng/dL [0.3 nmol/L]). (Reprinted, with permission, from reference 36.)
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Figure 11d. Ovarian carcinoid with testosterone-producing stroma in a 54-year-old woman. (a) Sagittal T2-weighted MR image shows a multilocular cystic mass with fluid of varying signal intensities in the lower abdomen. The mass contains a relatively large mural nodule (arrows), which has low signal intensity. (b) Sagittal contrast-enhanced T1-weighted MR image shows that the nodule has homogeneous enhancement (arrows). The patient had hirsutism and slight clitoromegaly. Laboratory data showed increased concentrations of serum testosterone (371.2 ng/dL [12.9 nmol/L]). Therefore, the preoperative radiologic diagnosis was a Sertoli-Leydig cell tumor. The cut surface of the resected specimen showed a multilocular cystic mass with a large white mural nodule. (c) Low-power photomicrograph (H-E stain) reveals medium-sized tumor cells proliferating in a solid and insular pattern accompanied by a delicate fibrous stroma. The tumor was positive for neuroendocrine markers at immunohistochemical staining, which helped determine the diagnosis of ovarian carcinoid. (d) High-power photomicrograph shows that the stroma is also positive for -inhibin stain (arrows), a finding that indicates that the stroma produces androgen. The serum testosterone level returned to normal after surgery (8.2 ng/dL [0.3 nmol/L]). (Reprinted, with permission, from reference 36.)
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Functioning stroma is seen most often in metastatic ovarian tumors (Fig 12). Metastatic ovarian tumors can appear as multilocular cystic masses or as mainly solid masses (37,38). They tend to be well-demarcated oval masses with various amounts of low-signal-intensity components on T2-weighted images (37). These MR imaging findings are somewhat similar to those seen in some parts of Sertoli-Leydig cell tumors (11) and GCTs (21). Radiologists should know that any type of ovarian tumor could have hormonal activity within its stroma and consider the possibility of tumors other than the more well-known hormone-producing tumors, especially in postmenopausal women.
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Abstract
Introduction
