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Tissue Characterization in the Female Pelvis by Means of MR Imaging¹

¹ From the Department of Radiology, University of Pennsylvania Medical Center, 1st Floor Silverstein, 3400 Spruce St, Philadelphia, PA 19104-4283 (E.S.S.), and the Department of Radiology, Thomas Jefferson University Hospital, Philadelphia, Pa (E.K.O.). Received July 16, 1998; revision requested August 28; revision received October 13; accepted February 10, 1999. Address reprint requests to E.S.S. (e-mail: siegelm@oasis.rad.upenn.edu).

Abstract

Pelvic imaging techniques such as computed tomography and ultrasonography provide a limited capability for tissue characterization. Fat, fluid, and calcification, for example, can be identified on the basis of parameters such as x-ray attenuation, echogenicity, and sound attenuation. Because of the many tissue parameters, such as T1, T2, magnetic susceptibility, and chemical shift, that contribute to signal intensity, magnetic resonance (MR) imaging may afford an ability to identify a wider array of specific tissues. The purpose of this article is to review the ability of MR imaging to help identify various types of soft tissue and to provide an approach to interpretation of MR images of the female pelvis through tissue characterization. Lipid, fluid, hemorrhage, smooth muscle, fibrosis, solid malignant tissue, and hydrated soft tissue (including edema, mucin, and myxomatous tissue) have typical MR imaging properties, and their presence in a mass can often be established on MR images. Consideration of the tissue composition of various pathologic processes in the pelvis can result in more systematic approaches to image interpretation and thus narrow the differential diagnosis.

Index terms: Magnetic resonance (MR), tissue characterization, 85.121412, 85.121413, 85.121414 • Pelvic organs, MR, 85.121412, 85.121413, 85.121414 • State-of-art reviews

Magnetic resonance (MR) imaging is emerging as a cost-effective technique for the evaluation of a variety of disorders of the female pelvis (1), including endometriosis (2) and cervical cancer (3). MR imaging of the pelvis in some clinical situations can obviate surgery or change a planned surgical procedure, alter medical treatment, and decrease health care costs (4), particularly after an inconclusive (5) sonogram of the adnexa has been obtained (4–6). Reviews of MR imaging of the female pelvis have detailed routine MR techniques and time-efficient protocols that use fast spin-echo (SE) sequences obtained in multiple planes and T1-weighted imaging with contrast material enhancement in selected cases (7–9).

The purpose of this article is to review the ability of MR imaging to help characterize tissue in the female pelvis. Our goal is to present a systematic approach to image interpretation through tissue characterization and not to describe an encyclopedic list of pelvic masses as seen on MR images. When interpreting an MR study of a female pelvis, one should often be able to determine what tissues are likely to compose a pathologic process. Tissue characterization is an important function of diagnostic radiologists ("the issue is tissue"); it is this aspect of image interpretation that often affects patient care. Computer-assisted MR tissue segmentation techniques have been developed that can anatomically locate and characterize specific soft-tissue types from a set of MR images (10–12). Similar analyses can often be done by radiologists when evaluating MR studies. The soft tissues that can often be characterized in the female pelvis include fluid, hemorrhage, lipid, smooth muscle, fibrosis, solid malignant tissue, and hydrated soft tissue (including mucin, myxoid tissue, and edematous tissue) (Table).

MR imaging findings other than size, location, and cystic solid composition are important in lesion characterization. What are the relative T1 and T2 signal intensities? What is the morphology of the mass? Is there loss of signal on fat-suppressed or chemical shift images? Is there signal loss from magnetic susceptibility effects on T2*-weighted images? Is enhancement present, and if so, what portions of the lesion enhance? Is there ascites and peritoneal enhancement? Assimilating the answers to the above questions can often determine what tissue(s) composes a detected abnormality.

Fluid
Fluid has characteristic imaging findings independent of its location in the body. Simple fluid has the longest T1 and longest T2 of any other tissue. Thus, static fluid has very low signal intensity on T1-weighted images and very high signal intensity on T2- and heavily T2-weighted images. By using a very long effective echo time with a T2-weighted sequence, fluid-containing structures in the pelvis remain hyperintense, while all other soft tissues show very low relative signal intensity. Such MR hydrograms (13), which can be obtained by using T2-weighted half-Fourier rapid acquisition with relaxation enhancement (RARE) imaging, are useful in the rapid evaluation of postoperative fluid collections and in the detection of an obstructed ureter (Fig 1) (14).

View larger version (106K): [in this window] [in a new window]   Figure 1. MR urography demonstrates obstruction of the distal ureter in a 49-year-old woman with surgically proved cervical carcinoma with parametrial invasion. Coronal maximum intensity projection MR urogram (/100) shows a dilated right collecting system and ureter to the level of the right ureterovesical junction (large straight arrow). Other fluid-containing structures include spinal fluid (curved arrow) and bowel (small straight arrow).

Fat-saturated T1-weighted images are recommended for the detection and characterization of hemorrhagic foci for several reasons. First, fat suppression decreases potential motion artifact from subcutaneous and intraabdominal fat. Second, a fat-saturated image distinguishes between fatty and hemorrhagic masses. Third, fat suppression improves the dynamic range of the image, with superior ability to distinguish small differences in signal intensity.

Characteristic MR imaging findings of a subacute hematoma has been termed the "concentric ring sign" (21–23). Often best delineated on fat-suppressed T1-weighted images, the concentric ring consists of an inner band of high signal intensity from methemoglobin and an outer low-signal-intensity rim from ferritin within macrophages. The outer low-signal-intensity ring is absent in early hematomas and in intraperitoneal hematomas (Figs 2, 3) (24,25). The ring sign is also absent in other hemorrhagic masses such as endometriomas and hemorrhagic functional cysts.

View larger version (177K): [in this window] [in a new window]   Figure 2. Blood within a subacute hematoma of rectus sheath and pelvis in a 76-year-old woman with atrial fibrillation who was being treated with oral anticoagulants. Axial fat-suppressed T1-weighted GRE image (300/1.7, 90° flip angle) shows typical left-sided rectus sheath and pelvic sidewall hematomas with a very high-signal-intensity outer rim (straight arrows) characteristic of methemoglobin. Magnetic susceptibility artifact (*) is present in the left femoral head from prior joint replacement. The unsuppressed fat (curved arrow) in the posterior acetabulum and deep gluteal soft tissues should not be interpreted as an additional site of hemorrhage.

View larger version (149K): [in this window] [in a new window]   Figure 3a. Blood present within an adnexal mass in a 17-year-old girl with ovarian torsion. Hemorrhagic infarction of the left ovary was confirmed at surgery. (a) Axial T1-weighted, fat-suppressed, spoiled GRE image (280/1.7, 90° flip angle) shows a 10-cm left adnexal mass that has a high-signal-intensity rim (arrows), suspicious for subacute hemorrhage. (b) Axial fat-suppressed T2-weighted fast SE image (4,600/98) obtained slightly higher throughout the mass shows scattered subcentimeter cysts (arrowheads) representing ovarian follicles. The remainder of the ovary is composed of low- to intermediate-signal-intensity material, likely representing deoxyhemoglobin. (c) Axial gadopentetate dimeglumine–enhanced, T1-weighted, fat-saturated GRE image obtained with identical imaging parameters as in a shows only faint rim enhancement (arrows) of the ovary. The remainder of the ovary shows no perfusion.

View larger version (135K): [in this window] [in a new window]   Figure 3b. Blood present within an adnexal mass in a 17-year-old girl with ovarian torsion. Hemorrhagic infarction of the left ovary was confirmed at surgery. (a) Axial T1-weighted, fat-suppressed, spoiled GRE image (280/1.7, 90° flip angle) shows a 10-cm left adnexal mass that has a high-signal-intensity rim (arrows), suspicious for subacute hemorrhage. (b) Axial fat-suppressed T2-weighted fast SE image (4,600/98) obtained slightly higher throughout the mass shows scattered subcentimeter cysts (arrowheads) representing ovarian follicles. The remainder of the ovary is composed of low- to intermediate-signal-intensity material, likely representing deoxyhemoglobin. (c) Axial gadopentetate dimeglumine–enhanced, T1-weighted, fat-saturated GRE image obtained with identical imaging parameters as in a shows only faint rim enhancement (arrows) of the ovary. The remainder of the ovary shows no perfusion.

View larger version (116K): [in this window] [in a new window]   Figure 3c. Blood present within an adnexal mass in a 17-year-old girl with ovarian torsion. Hemorrhagic infarction of the left ovary was confirmed at surgery. (a) Axial T1-weighted, fat-suppressed, spoiled GRE image (280/1.7, 90° flip angle) shows a 10-cm left adnexal mass that has a high-signal-intensity rim (arrows), suspicious for subacute hemorrhage. (b) Axial fat-suppressed T2-weighted fast SE image (4,600/98) obtained slightly higher throughout the mass shows scattered subcentimeter cysts (arrowheads) representing ovarian follicles. The remainder of the ovary is composed of low- to intermediate-signal-intensity material, likely representing deoxyhemoglobin. (c) Axial gadopentetate dimeglumine–enhanced, T1-weighted, fat-saturated GRE image obtained with identical imaging parameters as in a shows only faint rim enhancement (arrows) of the ovary. The remainder of the ovary shows no perfusion.

Subacute hematomas are commonly detected in the female pelvis in women after surgery (ie, cesarean delivery or oophorectomy) (28) and in women receiving anticoagulation therapy who present with pelvic pain and/or a palpable mass (Fig 2). In some postoperative patients, it can be difficult, if not impossible, to determine whether a hematoma is infected; aspiration and/or culture may be necessary in some patients. Subacute hematomas have also been described in women with ectopic pregnancy (29,30).

It has been suggested that in the setting of a pelvic hematoma, a hemorrhagic neoplasm should be excluded (30). However, hemorrhagic pelvic malignancies also contain solid, vascularized tissue and are distinguishable from masslike foci of bland hemorrhage (31).

Endometriosis.—Hemorrhagic foci within the ovary and pelvis are most commonly encountered in endometriosis. MR imaging can depict the presence of blood products within endometrial cysts (32) and usually distinguishes them from other hemorrhagic adnexal masses (33,34). The most common and specific appearance of endometrioma is a relatively homogeneous, high-signal-intensity cyst on T1-weighted images with low signal intensity on T2-weighted images (termed "shading") (Fig 4). Endometrial cysts are very hyperintense on T1-weighted images, similar to fat. The reasons for the characteristic low signal intensity of endometriomas on T2-weighted images may be related to their high iron content, which is 10–20 times the concentration of whole blood (35). Sugimura et al (35) found that 15 endometriomas had an iron concentration between 320 and 5,720 µg/dL (57 and 1,024 µmol/L), while the iron content of whole blood varied between 40 and 175 µg/dL (7 and 31 µmol/L). Increasing iron content of endometriomas corresponds with higher signal intensity on T1-weighted images (35) and lower signal intensity on T2-weighted images relative to the signal intensity of muscle (36).

View larger version (166K): [in this window] [in a new window]   Figure 4a. Adnexal endometrial cysts in a 37-year-old woman with surgically confirmed endometriosis. (a) Axial fat-suppressed T1-weighted GRE image (120/2.6, 60° flip angle) shows bilateral high-signal-intensity adnexal lesions (arrows). (b) Axial T2-weighted fast SE image (5,000/108) shows that the lesions are of low-signal-intensity "shading" (arrows). Bilateral adnexal lesions with high signal intensity on T1-weighted images and low signal intensity on T2-weighted images have high specificity for endometriosis.

View larger version (167K): [in this window] [in a new window]   Figure 4b. Adnexal endometrial cysts in a 37-year-old woman with surgically confirmed endometriosis. (a) Axial fat-suppressed T1-weighted GRE image (120/2.6, 60° flip angle) shows bilateral high-signal-intensity adnexal lesions (arrows). (b) Axial T2-weighted fast SE image (5,000/108) shows that the lesions are of low-signal-intensity "shading" (arrows). Bilateral adnexal lesions with high signal intensity on T1-weighted images and low signal intensity on T2-weighted images have high specificity for endometriosis.

Whereas pelvic hematomas have a variable appearance on both T1- and T2-weighted images as described above, hematomas will not mimic a typical endometrioma with diffusely high signal intensity on T1-weighted images and low signal intensity on T2-weighted images at any stage in development (25).

Hemorrhagic functional cysts and corpus luteum cysts.—High signal intensity on T1-weighted images in an ovarian cyst is not diagnostic of an endometrioma and is commonly seen in functional cysts. Hemorrhagic corpus luteum cysts are not uncommon in premenopausal women. MR imaging findings suggestive of a corpus luteum cyst include a unilateral, unifocal ovarian lesion and the presence of high signal intensity on T2-weighted images (Fig 5). The reason for the relative high signal intensity on T2-weighted images within hemorrhagic functional and corpus luteum cysts (as opposed to the lower signal intensity on T2-weighted images within endometriomas) presumably relates to the lower protein and iron content of the former, which results in minimal T2 shortening. Unlike endometrial cysts, corpus luteum cysts contain a layer of luteinized cells that line the cyst wall and that can appear thickened on MR imaging studies (7).

View larger version (160K): [in this window] [in a new window]   Figure 5a. Hemorrhagic corpus luteum cyst in a 41-year-old woman. (a) Axial T1-weighted SE image (500/16) shows a cyst with high signal intensity (arrow) in the left ovary. (b) Axial T2-weighted fast SE image (3,600/119) shows high signal intensity of the cyst. This combination of short T1 and long T2 is suggestive, but not diagnostic, of hemorrhagic functional cysts since some endometriomas can have a similar appearance (33). In our experience, the degree of T1 shortening is greater for endometriomas (Fig 4a) than for hemorrhagic functional cysts.

View larger version (172K): [in this window] [in a new window]   Figure 5b. Hemorrhagic corpus luteum cyst in a 41-year-old woman. (a) Axial T1-weighted SE image (500/16) shows a cyst with high signal intensity (arrow) in the left ovary. (b) Axial T2-weighted fast SE image (3,600/119) shows high signal intensity of the cyst. This combination of short T1 and long T2 is suggestive, but not diagnostic, of hemorrhagic functional cysts since some endometriomas can have a similar appearance (33). In our experience, the degree of T1 shortening is greater for endometriomas (Fig 4a) than for hemorrhagic functional cysts.

Adenomyosis.—Adenomyosis represents the presence of ectopic endometrial glands and stroma in the uterine myometrium (see "Smooth Muscle"). While less frequent than the ectopic endometrial glands of endometriosis, adenomyotic glands can bleed and result in high signal intensity on T1-weighted images (46,47).

Hematometrocolpos.—MR imaging is useful in the evaluation of primary amenorrhea and developmental uterine anomalies (48–50). Hematometrocolpos is the result of an imperforate hymen, transverse vaginal septum, or other obstruction to menstrual blood flow. MR imaging can noninvasively delineate the location and amount of retained blood (49,50) (Fig 6) and identify endometrial implants in the peritoneal cavity from retrograde menstruation. Blood in the dilated vagina or uterus with or without associated endometriosis (from retrograde menstruation) shows typical shading due to its chronic accumulation (Fig 6b).

View larger version (127K): [in this window] [in a new window]   Figure 6a. MR imaging demonstration of blood within a distended vagina and endocervical and endometrial canal in a 12-year-old girl with primary amenorrhea, pelvic pain, and a palpable pelvic mass. An obstructing low transverse vaginal septum was confirmed surgically. (a) Sagittal T1-weighted, fat-suppressed, GRE image (250/7, 90° flip angle) shows distention of the endometrial (*), endocervical (black arrow), and vaginal (V) canals by very high-signal-intensity material representing subacute blood. The level of the obstruction lies below the symphysis pubis, near the introitus (white arrow). (b) Sagittal T2-weighted fast SE image (4,000/105) shows low-signal-intensity "shading" of the hematometrocolpos. It can be difficult to differentiate an imperforate hymen from a low transverse septum at MR imaging.

View larger version (124K): [in this window] [in a new window]   Figure 6b. MR imaging demonstration of blood within a distended vagina and endocervical and endometrial canal in a 12-year-old girl with primary amenorrhea, pelvic pain, and a palpable pelvic mass. An obstructing low transverse vaginal septum was confirmed surgically. (a) Sagittal T1-weighted, fat-suppressed, GRE image (250/7, 90° flip angle) shows distention of the endometrial (*), endocervical (black arrow), and vaginal (V) canals by very high-signal-intensity material representing subacute blood. The level of the obstruction lies below the symphysis pubis, near the introitus (white arrow). (b) Sagittal T2-weighted fast SE image (4,000/105) shows low-signal-intensity "shading" of the hematometrocolpos. It can be difficult to differentiate an imperforate hymen from a low transverse septum at MR imaging.

Almost all lipid-containing masses within the adnexa are teratomas. Approximately 99% of teratomas are mature cystic teratomas (dermoid cysts) (55). The lipid content of dermoid cysts is largely sebaceous liquid material and less commonly adipose tissue. Immature teratomas are large cystic and solid tumors of children and young women and may also show small foci of fat.

Several techniques are available to characterize fat-containing structures in the pelvis. One method for establishing that tissue is composed of fat is through recognition of chemical shift misregistration in the frequency-encoding direction on SE images (56). Such a chemical shift effect with an SE sequence establishes that the boundary phenomenon is occurring at a fat-water interface (Fig 7). A second method for establishing the lipid content of a pelvic mass is to compare T1-weighted images obtained before and after a proton-selective fat saturation or water saturation pulse. If a mass loses signal after fat saturation or has persistent signal after water saturation, then the mass contains fat. Both fat (Fig 8c) and water saturation techniques (Fig 8d) (57) enable detection and characterization of dermoid cysts and distinguish them from other processes that have high signal intensity on T1-weighted images (38,58–61).

View larger version (136K): [in this window] [in a new window]   Figure 7. Fat within a left adnexal mass in a 37-year-old woman with a surgically confirmed mature teratoma. Axial T2-weighted fast SE image (5,000/102) shows a complex mass with a meniscoid tissue–fluid level that is separated by a low-signal-intensity boundary (arrows). The latter likely represents a chemical shift in the frequency-encoding direction (anterior-to-posterior) at a fat-water interface. A spherical central portion of the mass is present. This sequence alone, while sufficient to establish a diagnosis of a teratoma, should be confirmed with either a fat saturation, water saturation, or chemical shift technique.

View larger version (164K): [in this window] [in a new window]   Figure 8. Varying amounts of fat within a right-sided mature teratoma in a 41-year-old woman. A, Axial T1-weighted, in-phase, spoiled GRE image (120/4.2, 90° flip angle) shows a right adnexal mass with a very high-signal-intensity anterior component (straight arrow) and an intermediate- to high-signal-intensity posterior component (curved arrow). B, Axial T1-weighted, opposed-phase, spoiled GRE image (120/2.1, 90° flip angle) shows marked signal loss in the posterior portion of the mass, establishing the presence of microscopic lipid. While there is no signal loss of the anterior component of the mass, there is a subtle etching artifact at the border between the anterior aspect of the mass and the surrounding ovarian and paraovarian tissue (arrows). C, Axial T1-weighted, fat-saturated, opposed-phase, spoiled GRE image (120./2.1, 90o flip angle) shows marked loss of signal in the anterior portion of the mass, establishing the presence of macroscopic fat. Compared to the in-phase image in A, it is difficult to appreciate any change in signal intensity in the posterior portion of the mass. D, Axial T1-weighted, water-saturated spoiled GRE image (120/4.2, 90° flip angle) shows the macroscopic fat anteriorly and microscopic lipid posteriorly. This mature teratoma in a 41-year-old woman illustrates the complementary use of fat saturation and in-phase–opposed-phase chemical shift techniques in the characterization of lipid-containing masses.

Some cystic teratomas do not have abundant lipid but instead contain smaller amounts of adipocytes or tissue with intracellular lipid (63). Chemical shift imaging using GRE techniques is a more sensitive method for detecting the presence of small amounts of lipid within such masses (64) (Fig 8a, 8b). By demonstrating loss of signal on an opposed-phase image compared to an in-phase image, chemical shift MR imaging techniques can depict the lipid content of teratomas (7) and perform as well as standard fat-saturation techniques (65). The latter methods result in greater signal loss in masses composed almost entirely of fat, while the former methods are more sensitive for suppressing microscopic lipid.

Macromolecules
To understand the relative signal intensity of tissues composed of macromolecules, a brief review of the biologic states of water is necessary (66–69). Water can exist in either a free or bound state. Free water has unrestricted motion, whereas bound water (for example water molecules that are associated with intracellular proteins) has restricted motion. The hydrogen protons of bound water tumble with a frequency closer to the Larmor frequency and are more efficient at T1 relaxation and T2 decay. This results in shortening of both the T1 and T2 relaxation times of the water. While this mechanism of T1 and T2 shortening occurs to some extent in all tissues, there are several subtypes of soft tissue, such as muscle and fibrous tissue, that are composed of a large proportion of macromolecules. Their relative signal intensities may provide insight into their tissue components.

Magnetization transfer effects are a second phenomenon that results in lower signal intensity of macromolecular-rich soft tissues on T2-weighted images, especially when using fast SE techniques that employ multiple refocusing pulses. The latter pulses result in increased off-resonance radio-frequency energy, which saturates protons bound to macromolecules (43,62).

Smooth Muscle
Compared to other soft tissues in the body, both smooth muscle and skeletal muscle have low signal intensity on T2-weighted images, which results from the T2 shortening effects of intramuscular actin, myosin, and collagen and decreased extracellular fluid compared with surrounding tissues (70–72). Normal structures in the pelvis that have very low signal intensity on T2-weighted images include the junctional zone of the uterus; the vaginal, urethral, and rectal muscularis; and the bladder detrusor muscle.

The smooth-muscle composition of the uterine myometrium has been studied with MR imaging. The junctional zone (inner myometrium) of the uterus is both functionally and structurally different from the outer myometrium (73). The normal junctional zone has lower signal intensity on T2-weighted images than that of the adjacent outer myometrium (Figs 4, 9, 10). The outer myometrium has higher signal intensity because of less compact smooth muscle, greater extracellular matrix, increased water content, and more numerous venous structures (74,75). Focal myometrial contractions cause more compact smooth muscle with compressed venous structures and thus can mimic either leiomyoma or focal adenomyosis on MR imaging studies (76). Situations in which contractions are seen are during pregnancy (77) and less typically during any phase of the menstrual cycle (78). Documenting the transient nature of the pseudomass will establish the diagnosis (Fig 11).

View larger version (187K): [in this window] [in a new window]   Figure 9. MR imaging demonstration of fibrotic bilateral adnexal masses and smooth-muscle myometrial masses in a 73-year-old woman with bilateral fibrothecomas, endometrial hyperplasia, and uterine leiomyomas. Axial T2-weighted fast SE image (5,000/136) shows bilateral adnexal masses (white *) whose signal intensity is lower than that of the outer myometrium and isointense to minimally hyperintense compared with the normal junctional zone and pelvic musculature. There is a widened endometrial complex (black *) and clear definition of the inner and outer myometrium, both of which are suggestive of hormonal production by the tumors in this postmenopausal woman. Three well-circumscribed, low-signal-intensity myometrial masses are present. One has a submucosal component (black arrow), another has a high-signal-intensity rim (solid white arrow), and the third has high signal intensity internally (open white arrow).

View larger version (162K): [in this window] [in a new window]   Figure 10a. MR imaging demonstration of enhancing solid cancer with spread to the peritoneum in a 41-year-old woman with a surgically confirmed malignant epithelial ovarian neoplasm with peritoneal spread of disease. (a) Axial T2-weighted fast SE image (5,800/126) shows a large complex right adnexal mass with both cystic and solid components. The solid components are of higher signal intensity than that of the uterine myometrium. Solid projections of tissue (small arrows) within one of the intratumoral cysts and nodules of soft-tissue signal intensity (large arrow) are present in the cul-de-sac. (b) Axial gadopentetate dimeglumine–enhanced fat-saturated GRE image (400/2.9, 90° flip angle) shows enhancing intracystic solid tissue (small arrows) and peritoneal implants (large arrow).

View larger version (167K): [in this window] [in a new window]   Figure 10b. MR imaging demonstration of enhancing solid cancer with spread to the peritoneum in a 41-year-old woman with a surgically confirmed malignant epithelial ovarian neoplasm with peritoneal spread of disease. (a) Axial T2-weighted fast SE image (5,800/126) shows a large complex right adnexal mass with both cystic and solid components. The solid components are of higher signal intensity than that of the uterine myometrium. Solid projections of tissue (small arrows) within one of the intratumoral cysts and nodules of soft-tissue signal intensity (large arrow) are present in the cul-de-sac. (b) Axial gadopentetate dimeglumine–enhanced fat-saturated GRE image (400/2.9, 90° flip angle) shows enhancing intracystic solid tissue (small arrows) and peritoneal implants (large arrow).

View larger version (127K): [in this window] [in a new window]   Figure 11a. MR imaging demonstration of a focal myometrial contraction. (a, b) Sagittal T2-weighted half-Fourier RARE images (/96) obtained 25 minutes apart in a 32-year-old woman shows fetal head, chest, and abdominal contents to good advantage. A transient low-signal-intensity mass of the anterior uterine wall (*) represents a focal myometrial contraction. Half-Fourier RARE techniques have allowed one to obtain fetal MR images that are relatively free of motion artifacts (79,80).

View larger version (139K): [in this window] [in a new window]   Figure 11b. MR imaging demonstration of a focal myometrial contraction. (a, b) Sagittal T2-weighted half-Fourier RARE images (/96) obtained 25 minutes apart in a 32-year-old woman shows fetal head, chest, and abdominal contents to good advantage. A transient low-signal-intensity mass of the anterior uterine wall (*) represents a focal myometrial contraction. Half-Fourier RARE techniques have allowed one to obtain fetal MR images that are relatively free of motion artifacts (79,80).

View larger version (187K): [in this window] [in a new window]   Figure 12. MR imaging demonstration of diffuse smooth-muscle proliferation within the inner myometrium in a 36-year-old woman with adenomyosis. Sagittal T2-weighted fast SE image (4,200/108) shows diffuse asymmetric thickening of the inner myometrium by a relatively low-signal-intensity process (black arrows) compared to the outer myometrium. Punctate foci of high signal intensity (white arrows) are present. The diffuse area of low signal intensity within the myometrium represents reactive smooth-muscle proliferation. The ectopic intramyometrial endometrial glands have high signal intensity on this T2-weighted image.

View larger version (119K): [in this window] [in a new window]   Figure 13a. Invasive squamous cell carcinoma of the cervix in a 64-year-old woman with vaginal bleeding . (a) Sagittal T2-weighted fast SE image (3,500/90) shows an infiltrative intermediate-signal-intensity cervical mass that invades the vagina (white arrow), posterior bladder wall (black arrow), and uterine body. Two low-signal-intensity leiomyomas (arrowheads) are clearly delineated. (b) Sagittal T2-weighted half-Fourier RARE image (/98) shows blurring of the margins of the cancer and the leiomyomas, secondary to T2 decay during the long echo train (83,84). An optimized fast SE sequence is preferred to a corresponding half-Fourier RARE sequence in the evaluation of normal uteri, because of the latter sequence's limitations on contrast and signal-to-noise ratio (85). However, a diagnosis of bladder invasion can still be established in this instance.

View larger version (117K): [in this window] [in a new window]   Figure 13b. Invasive squamous cell carcinoma of the cervix in a 64-year-old woman with vaginal bleeding . (a) Sagittal T2-weighted fast SE image (3,500/90) shows an infiltrative intermediate-signal-intensity cervical mass that invades the vagina (white arrow), posterior bladder wall (black arrow), and uterine body. Two low-signal-intensity leiomyomas (arrowheads) are clearly delineated. (b) Sagittal T2-weighted half-Fourier RARE image (/98) shows blurring of the margins of the cancer and the leiomyomas, secondary to T2 decay during the long echo train (83,84). An optimized fast SE sequence is preferred to a corresponding half-Fourier RARE sequence in the evaluation of normal uteri, because of the latter sequence's limitations on contrast and signal-to-noise ratio (85). However, a diagnosis of bladder invasion can still be established in this instance.

Solid masses of endometriosis.—Solid fibrotic masses or nodules of endometriosis are composed of reactive fibrosis surrounding glands of endometriosis. They appear as spiculated masses that have low signal intensity on T2-weighted images sometimes with punctate high signal intensity on T1-weighted images (92). Fibrotic masses of endometriosis affect the cul-de-sac, bladder, and rectum and are also encountered in the anterior abdominal wall in women after a cesarean delivery (93).

Fibromas and fibrothecomas.—Fibromas are composed of spindle cells that produce a variable amount of collagen and are not hormonally active. Fibrothecomas contain both fibrous tissue and theca cells and are often hormonally active. The fibrous tissue that composes the majority of most of these tumors is responsible for the low signal intensity delineated on both T1- and T2-weighted images (Fig 9). Intratumoral edema is also common in larger fibromas, which explains why many fibromas are not uniformly hypointense on T2-weighted images (94). A widened endometrial stripe in association with an ovarian mass with low signal intensity on T2-weighted images can suggest a diagnosis of functioning fibrothecoma with endometrial hyperplasia (95) (Fig 9).

Cystadenofibroma.—Cystadenofibromas are a subset of epithelial ovarian neoplasms that are usually benign. The presence of rims, plaques, or nodules that have low signal intensity on T2-weighted images and that range in size between 2 mm and 4 cm within a multiloculated cystic ovarian mass can suggest the diagnosis (95). As is the case for fibromas, the low-signal-intensity foci correspond to intratumoral regions of dense fibrous tissue.

Brenner tumor.—Benign transitional cell (Brenner) tumors of the ovary compose approximately 2% of epithelial ovarian neoplasms. Brenner tumors are often discovered incidentally at surgery or pathologic examination because they are small and asymptomatic (96). In 30% of cases, Brenner tumors are associated with an epithelial ovarian neoplasm of either the ipsilateral or contralateral ovary (Fig 14). Brenner tumors contain abundant fibrous stroma (96), which accounts for the low signal intensity on T2-weighted images in those masses visible on MR images (Fig 14) (97). Brenner tumors also contain small epithelial nests that are too small to visualize as high-signal-intensity foci on T2-weighted images.

View larger version (162K): [in this window] [in a new window]   Figure 14a. MR imaging demonstration of fibrous tissue and mucin within a complex left adnexal mass in a 51-year-old woman. At surgery, the fibrous mass was a Brenner tumor and the mucin-containing mass was a borderline mucinous tumor. (a) Axial T1-weighted SE (400/10) and (b) T2-weighted fast SE (4,700/85) images show a large pelvic mass that displaces the uterus (curved arrow in b) posteriorly. The mass has two components. Anteriorly and laterally, there is a well-circumscribed, 6.5-cm mass (white *) that has low signal intensity on both the T1- and T2-weighted images. The remainder of the mass has low-, intermediate-, and high- (black * in a) signal-intensity components relative to muscle on the T1-weighted image and intermediate- to high-signal-intensity components on the T2-weighted image. (MR images courtesy of Bohyun Kim, MD, Samsung Medical Center, Seoul, Korea.)

View larger version (168K): [in this window] [in a new window]   Figure 14b. MR imaging demonstration of fibrous tissue and mucin within a complex left adnexal mass in a 51-year-old woman. At surgery, the fibrous mass was a Brenner tumor and the mucin-containing mass was a borderline mucinous tumor. (a) Axial T1-weighted SE (400/10) and (b) T2-weighted fast SE (4,700/85) images show a large pelvic mass that displaces the uterus (curved arrow in b) posteriorly. The mass has two components. Anteriorly and laterally, there is a well-circumscribed, 6.5-cm mass (white *) that has low signal intensity on both the T1- and T2-weighted images. The remainder of the mass has low-, intermediate-, and high- (black * in a) signal-intensity components relative to muscle on the T1-weighted image and intermediate- to high-signal-intensity components on the T2-weighted image. (MR images courtesy of Bohyun Kim, MD, Samsung Medical Center, Seoul, Korea.)

HYDRATED TISSUE

Mucin
Mucin is a secretion that contains carbohydrate-rich glycoproteins. Hydrated mucinous tissue is of low viscosity and in general has low signal intensity on T1-weighted images and high signal intensity on T2-weighted images. In desiccated mucinous secretions, the decrease in free water can result in marked T2 shortening (68), which can be so pronounced that it also results in very low signal intensity on T1-weighted images (104). This latter phenomenon has not been encountered in the pelvis but has been documented in the paranasal sinuses (105).

Mucinous ovarian neoplasms.—Mucinous neoplasms of the ovary compose approximately one-third of epithelial ovarian tumors, and approximately 80% are benign (89). Benign tumors are commonly large, so size does not strongly correlate with the probability of malignancy in this type of tumor. At gross examination, mucinous neoplasms are multilocular and the cyst contents vary from a low-viscosity waterlike consistency to a thick viscous material from concentrated mucin. The latter cyst contents can result in variable T1 shortening within some locules. T2 shortening is usually slight (Figs 14, 15). Unilocular mucinous neoplasms may be indistinguishable from other adnexal cysts.

View larger version (146K): [in this window] [in a new window]   Figure 15a. MR imaging demonstration of various concentrations of mucin within a mucinous neoplasm of low malignant potential of the right ovary in a 37-year-old woman. (a) Axial T1-weighted SE image (600/12) demonstrates a large multilocular cystic mass with varying signal intensities that are hypointense (large white *), minimally hyperintense (small white *), and markedly hyperintense (black *) relative to muscle. (b) Axial T2-weighted fast SE image (6,000/126) shows that the majority of the locules are moderately hyperintense to muscle. The lack of solid components, ascites, or peritoneal implants suggests a benign diagnosis.

View larger version (120K): [in this window] [in a new window]   Figure 15b. MR imaging demonstration of various concentrations of mucin within a mucinous neoplasm of low malignant potential of the right ovary in a 37-year-old woman. (a) Axial T1-weighted SE image (600/12) demonstrates a large multilocular cystic mass with varying signal intensities that are hypointense (large white *), minimally hyperintense (small white *), and markedly hyperintense (black *) relative to muscle. (b) Axial T2-weighted fast SE image (6,000/126) shows that the majority of the locules are moderately hyperintense to muscle. The lack of solid components, ascites, or peritoneal implants suggests a benign diagnosis.

Other mucin-producing adenocarcinomas.—Mucin-producing adenocarcinomas show high signal intensity on T2-weighted images from the extracellular mucin of the primary lesion (Fig 16). Nonmucinous adenocarcinomas have substantially lower signal intensity than that of mucinous tumors on T2-weighted images, although they still are of higher signal intensity than that of skeletal muscle (110). After administration of contrast material, mucinous malignancies show lacelike internal enhancement, which distinguishes them from cysts or abscesses. This is most conspicuous with fat-suppressed T1-weighted techniques.

View larger version (160K): [in this window] [in a new window]   Figure 16a. MR imaging demonstration of mucin within recurrent mucinous adenocarcinoma of the rectum in a 65-year-old woman. (a) Axial fat-suppressed T2-weighted fast SE (3,000/99) and (b) gadopentetate dimeglumine–enhanced fat-saturated GRE (200/2.9, 90° flip angle) images show an infiltrative heterogeneous mass that has high signal intensity on the T2-weighted image; the center of the mass is in the rectal bed. There is a fistula to the left vaginal fornix (*). There is heterogeneous peripheral enhancement and patchy internal enhancement that distinguishes this process from a postprocedural fluid collection. Both the high signal intensity of the rectal tumor on the T2-weighted image and the irregular rim enhancement are very suggestive of a mucinous subtype of rectal carcinoma (110). (c) Histologic section of the mass shows glandular epithelium (arrow) with abundant extracellular mucin (*). (Hematoxylin-eosin stain; original magnification, x20.)

View larger version (173K): [in this window] [in a new window]   Figure 16b. MR imaging demonstration of mucin within recurrent mucinous adenocarcinoma of the rectum in a 65-year-old woman. (a) Axial fat-suppressed T2-weighted fast SE (3,000/99) and (b) gadopentetate dimeglumine–enhanced fat-saturated GRE (200/2.9, 90° flip angle) images show an infiltrative heterogeneous mass that has high signal intensity on the T2-weighted image; the center of the mass is in the rectal bed. There is a fistula to the left vaginal fornix (*). There is heterogeneous peripheral enhancement and patchy internal enhancement that distinguishes this process from a postprocedural fluid collection. Both the high signal intensity of the rectal tumor on the T2-weighted image and the irregular rim enhancement are very suggestive of a mucinous subtype of rectal carcinoma (110). (c) Histologic section of the mass shows glandular epithelium (arrow) with abundant extracellular mucin (*). (Hematoxylin-eosin stain; original magnification, x20.)

View larger version (181K): [in this window] [in a new window]   Figure 16c. MR imaging demonstration of mucin within recurrent mucinous adenocarcinoma of the rectum in a 65-year-old woman. (a) Axial fat-suppressed T2-weighted fast SE (3,000/99) and (b) gadopentetate dimeglumine–enhanced fat-saturated GRE (200/2.9, 90° flip angle) images show an infiltrative heterogeneous mass that has high signal intensity on the T2-weighted image; the center of the mass is in the rectal bed. There is a fistula to the left vaginal fornix (*). There is heterogeneous peripheral enhancement and patchy internal enhancement that distinguishes this process from a postprocedural fluid collection. Both the high signal intensity of the rectal tumor on the T2-weighted image and the irregular rim enhancement are very suggestive of a mucinous subtype of rectal carcinoma (110). (c) Histologic section of the mass shows glandular epithelium (arrow) with abundant extracellular mucin (*). (Hematoxylin-eosin stain; original magnification, x20.)

Angiomyxoma.—Angiomyxoma is an unusual neoplasm that characteristically arises within the mesenchymal tissues of the pelvis and perineum of young women. The tumor is benign but often recurs locally. A suggestive MR imaging finding is that of an infiltrative soft-tissue mass of the female pelvis and/or perineum of very high signal intensity on T2-weighted images that tends to displace, but not invade, adjacent soft-tissue structures (49,117,118).

Myxoid degeneration of uterine leiomyomas.—Myxomatous change is one subtype of degeneration that occurs in uterine leiomyomas, especially in larger masses (112,119) (Fig 17). Myxoid change appears as a geographic patchwork of very high signal intensity within a leiomyoma. Characterization of the subtypes of degeneration within uterine leiomyomas is often not necessary for lesion characterization. However, knowledge of the degree and subtype of degeneration may influence the decision to treat a symptomatic women with medical therapy. Degenerated tumors do not respond to medical therapy, whereas nondegenerated leiomyomas shrink in size (86).

View larger version (180K): [in this window] [in a new window]   Figure 17a. Myxoid tissue in a degenerated leiomyoma in a 49-year-old woman. (a) Sagittal and (b) axial T2-weighted fast SE images (5,300/126) show a well-circumscribed mass of the anterior uterus that has both low- (white * in b) and high- (black * in b) signal-intensity components compared to the outer myometrium. (c) Gadopentetate dimeglumine–enhanced fat-saturated GRE image (500/3.3, 90° flip angle) obtained at the same level as b shows that some of the intratumoral tissue with high signal intensity on the T2-weighted image enhances, indicating that it does not represent intratumoral cysts or necrosis. (d) Histologic section of a different myxoid leiomyoma shows the loose, water-laden myxoid tissue (*) contrasted with the denser smooth-muscle bundles of the leiomyomas (thick arrow). Myxoid degeneration is not necrosis; several vessels (thin arrows) still course through the myxoid tissue. (Hematoxylin-eosin stain; original magnification, x40.)

View larger version (171K): [in this window] [in a new window]   Figure 17b. Myxoid tissue in a degenerated leiomyoma in a 49-year-old woman. (a) Sagittal and (b) axial T2-weighted fast SE images (5,300/126) show a well-circumscribed mass of the anterior uterus that has both low- (white * in b) and high- (black * in b) signal-intensity components compared to the outer myometrium. (c) Gadopentetate dimeglumine–enhanced fat-saturated GRE image (500/3.3, 90° flip angle) obtained at the same level as b shows that some of the intratumoral tissue with high signal intensity on the T2-weighted image enhances, indicating that it does not represent intratumoral cysts or necrosis. (d) Histologic section of a different myxoid leiomyoma shows the loose, water-laden myxoid tissue (*) contrasted with the denser smooth-muscle bundles of the leiomyomas (thick arrow). Myxoid degeneration is not necrosis; several vessels (thin arrows) still course through the myxoid tissue. (Hematoxylin-eosin stain; original magnification, x40.)

View larger version (176K): [in this window] [in a new window]   Figure 17c. Myxoid tissue in a degenerated leiomyoma in a 49-year-old woman. (a) Sagittal and (b) axial T2-weighted fast SE images (5,300/126) show a well-circumscribed mass of the anterior uterus that has both low- (white * in b) and high- (black * in b) signal-intensity components compared to the outer myometrium. (c) Gadopentetate dimeglumine–enhanced fat-saturated GRE image (500/3.3, 90° flip angle) obtained at the same level as b shows that some of the intratumoral tissue with high signal intensity on the T2-weighted image enhances, indicating that it does not represent intratumoral cysts or necrosis. (d) Histologic section of a different myxoid leiomyoma shows the loose, water-laden myxoid tissue (*) contrasted with the denser smooth-muscle bundles of the leiomyomas (thick arrow). Myxoid degeneration is not necrosis; several vessels (thin arrows) still course through the myxoid tissue. (Hematoxylin-eosin stain; original magnification, x40.)

View larger version (187K): [in this window] [in a new window]   Figure 17d. Myxoid tissue in a degenerated leiomyoma in a 49-year-old woman. (a) Sagittal and (b) axial T2-weighted fast SE images (5,300/126) show a well-circumscribed mass of the anterior uterus that has both low- (white * in b) and high- (black * in b) signal-intensity components compared to the outer myometrium. (c) Gadopentetate dimeglumine–enhanced fat-saturated GRE image (500/3.3, 90° flip angle) obtained at the same level as b shows that some of the intratumoral tissue with high signal intensity on the T2-weighted image enhances, indicating that it does not represent intratumoral cysts or necrosis. (d) Histologic section of a different myxoid leiomyoma shows the loose, water-laden myxoid tissue (*) contrasted with the denser smooth-muscle bundles of the leiomyomas (thick arrow). Myxoid degeneration is not necrosis; several vessels (thin arrows) still course through the myxoid tissue. (Hematoxylin-eosin stain; original magnification, x40.)

The normal ovary has a zonal anatomy consisting of an outer ovarian cortex and central ovarian medulla that along with the follicles compose the internal contents of the ovary. In premenopausal patients, ovarian zonal anatomy is distinguishable on T2-weighted images (39,124). At histologic examination, ovarian stroma in the cortex is more cellular (125), while medullary stroma is composed of looser, vascularized connective tissue with a higher free water content, thus explaining the difference in contrast on T2-weighted images (39).

Massive edema of the ovary.—In a subset of intermittently or partially twisted, viable ovaries, a characteristic appearance of enlargement from ovarian edema without hemorrhage is termed "massive ovarian edema" (126–129). Similar to adnexal torsion, follicles are displaced peripherally, but unlike torsion, the ovarian stroma is edematous and of high signal intensity on T2-weighted images (Fig 18). In these women, laparoscopic oophoropexy can be performed instead of an oophorectomy, thus preserving fertility (130).

View larger version (148K): [in this window] [in a new window]   Figure 18a. MR imaging appearance of ovarian edema without hemorrhage in a 16-year-old girl with pelvic pain. At subsequent surgery, a partially twisted, viable left ovary (massive ovarian edema) was present. (a) Fat-suppressed, T2-weighted fast SE image (4,600/133) shows a large left adnexal mass that contains multiple follicles (black arrows), identifying it as the left ovary. A prominent right ovary (white arrow) is also present. (b) Gadopentetate dimeglumine–enhanced axial fat-suppressed T1-weighted spoiled GRE image (150/2.9, 90° flip angle) shows enhancing follicles within both ovaries (arrows). No high signal intensity was present on the T1-weighted images before administration of contrast material (not shown) to suggest hemorrhagic infarction (see Fig 3).

View larger version (158K): [in this window] [in a new window]   Figure 18b. MR imaging appearance of ovarian edema without hemorrhage in a 16-year-old girl with pelvic pain. At subsequent surgery, a partially twisted, viable left ovary (massive ovarian edema) was present. (a) Fat-suppressed, T2-weighted fast SE image (4,600/133) shows a large left adnexal mass that contains multiple follicles (black arrows), identifying it as the left ovary. A prominent right ovary (white arrow) is also present. (b) Gadopentetate dimeglumine–enhanced axial fat-suppressed T1-weighted spoiled GRE image (150/2.9, 90° flip angle) shows enhancing follicles within both ovaries (arrows). No high signal intensity was present on the T1-weighted images before administration of contrast material (not shown) to suggest hemorrhagic infarction (see Fig 3).

View larger version (141K): [in this window] [in a new window]   Figure 19a. MR imaging demonstration of papillary projections in a papillary serous borderline tumor in a 19-year-old woman. (a) Axial T2-weighted fast SE image (4,000/126) shows a complex multiloculated pelvic mass that contains multiple papillary projections. The projections in the left cyst are composed of a central fibrous core (long black arrow) surrounded by edematous stroma (short black arrows). The right-sided mass (curved white arrow) is a cyst filled entirely with papillary projections. (b) Corresponding axial gadopentetate dimeglumine–enhanced fat-saturated GRE image (250/2.9, 90° flip angle) shows enhancement of the cyst wall (arrow) and papillary projections. The fluid that makes up the remainder of the tumor does not enhance.

View larger version (151K): [in this window] [in a new window]   Figure 19b. MR imaging demonstration of papillary projections in a papillary serous borderline tumor in a 19-year-old woman. (a) Axial T2-weighted fast SE image (4,000/126) shows a complex multiloculated pelvic mass that contains multiple papillary projections. The projections in the left cyst are composed of a central fibrous core (long black arrow) surrounded by edematous stroma (short black arrows). The right-sided mass (curved white arrow) is a cyst filled entirely with papillary projections. (b) Corresponding axial gadopentetate dimeglumine–enhanced fat-saturated GRE image (250/2.9, 90° flip angle) shows enhancement of the cyst wall (arrow) and papillary projections. The fluid that makes up the remainder of the tumor does not enhance.

Malignant tissue has increased amounts of both intracellular and extracellular water, which results in increased T1 and T2 relaxation times of malignant tissue (66,131) (Figs 10, 13, 19). However, whether this results in a relatively higher signal intensity on T2-weighted images compared to the signal intensity of background tissue depends on the comparison tissue. For example, endometrial cancer usually has lower signal intensity compared with that of normal endometrium. On fast SE images, fat signal intensity is typically equal to or higher than the signal intensity of malignant tissue. The relative T2 signal intensity of soft tissue is also dependent on the degree of T2 weighting. For example, when performing heavily T2-weighted sequences (MR hydrography [13]), most soft tissues are of very low signal intensity with minimal or no difference in tissue contrast (Fig 1). Therefore, one cannot always rely on the relative T2 signal intensity of a mass to suggest malignancy. However, many organs in the female pelvis contain a layer with low signal intensity on T2-weighted images—for example, uterine junctional zone, cervical stroma (132), urethral muscularis (133), and bladder wall (Fig 13) (134,135)—so that malignancies show higher signal intensity than these structures. Masses that extend through these low-signal-intensity mural layers are suggestive of invasive disease.

In addition to evidence of invasion, the presence of serosal implants suggests a diagnosis of malignancy and excludes benign disease. Gadolinium-enhanced, breath-hold, fat-saturated T1-weighted gradient-echo imaging performed after the ingestion of a dilute barium suspension has been shown to accurately detect serosal disease from pelvic malignancies (double contrast MR imaging) (136,137). It is still unclear whether intraluminal barium improves sensitivity since similar detection rates of serosal disease have also been demonstrated with an identical sequence without an orally administered contrast material (138) (Fig 10). Peritoneal disease with a pelvic mass does not necessarily indicate spread of pelvic malignancy, however, and can be seen in endometriosis and borderline tumors.

When evaluating adnexal masses specifically, the presence of papillary projections adds high specificity for an epithelial ovarian neoplasm (Fig 19) (7,37). The presence and quantity of papillary projections can suggest the degree of tumor invasiveness. Papillary projections are usually absent in benign epithelial neoplasms and abundant within borderline tumors. Solid tumor is usually present in greater proportion than papillary projections within ovarian malignancies (139,140).

CONCLUSION

This article provides an approach to interpretation of MR images of the female pelvis through tissue characterization. Fluid, blood, lipid, smooth muscle, fibrous tissue, mucin, myxomatous tissue, and solid neoplastic tissue have typical signal intensity and enhancement patterns that can be recognized. Identification of these tissue types in a mass can narrow the differential diagnosis. It is our hope that the MR imaging information of tissue composition of various pathologic processes in the pelvis can result in more systematic approaches to diagnosis.

Footnotes

Abbreviations: GRE = gradient-recalled echo RARE = rapid acquisition with relaxation enhancement SE = spin echo STIR = short inversion time inversion recovery

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