(Radiographics. 1999;19:937-945.)
© RSNA, 1999
Staging of Early Endometrial Carcinoma: Assessment with T2-weighted and Gadolinium-enhanced T1-weighted MR Imaging1
Eun Jung Lee, MD,
Jae Young Byun, MD,
Bum-soo Kim, MD,
Sung E. Nam Koong, MD and
Kyung Sub Shinn, MD
1 From the Departments of Radiology (E.J.L., J.Y.B., B.K., K.S.S.) and Obstetrics and Gynecology (S.E.N.K.), Kangnam St Mary's Hospital, Catholic University of Korea, 505 Banpo-dong, Seocho-ku, Seoul 137-040, Korea. Presented as a scientific exhibit at the 1997 RSNA scientific assembly. Received June 10, 1998; revision requested August 24; final revision received November 10; accepted November 10. Address reprint requests to J.Y.B.
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Abstract
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This study evaluated the usefulness of T2-weighted and gadolinium-enhanced T1-weighted magnetic resonance (MR) images correlated with patients' menopausal status in assessing the depth of myometrial invasion in stage I endometrial carcinoma. MR images of 46 patients with stage I endometrial carcinoma were retrospectively reviewed. Twenty-five patients were premenopausal, and 21 were postmenopausal. The staging accuracy without regard to menopausal status was 59% for T2-weighted images and 61% for gadolinium-enhanced T1-weighted images. However, when staging accuracy was evaluated separately in the premenopausal and postmenopausal patient groups, T2-weighted imaging had an accuracy of 80% in the premenopausal group and gadolinium-enhanced T1-weighted imaging had an accuracy of 81% in the postmenopausal group. Therefore, T2-weighted imaging was more accurate in premenopausal patients and gadolinium-enhanced T1-weighted imaging was more accurate in postmenopausal patients. The overall accuracy of staging with MR imaging improved to 80% when patients' menopausal status was considered. Therefore, menopausal status should be considered when T2-weighted and gadolinium-enhanced T1-weighted MR images are used to stage early endometrial carcinoma.
Index Terms: Uterine neoplasms, MR, 854.12143, 854.32 • Uterine neoplasms, staging, 854.32
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INTRODUCTION
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Endometrial carcinoma is the most common gynecologic malignant neoplasm in the United States (1). About 80% of cases are diagnosed while still in the early stage because early symptoms include vaginal spotting or bleeding (2,3). The prognosis of endometrial carcinoma depends on the depth of myometrial invasion and the presence of lymph node metastasis. Myometrial extension is a reliable index of lymphatic spread. Preoperative assessment of myometrial invasion is important in planning the surgical procedure and determining whether to perform lymph node sampling (2–4). Patients with lymph node metastases have a significantly higher recurrence rate and a lower 5-year survival rate than those without lymph node metastases (5).
For proper surgical and therapeutic planning, magnetic resonance (MR) imaging has been used preoperatively to evaluate myometrial invasion with relatively high accuracy (6–13). Previous studies have suggested that gadolinium-enhanced MR imaging is even more accurate in assessing myometrial invasion by endometrial cancer (6–8). Therefore, we evaluated the accuracy of T2-weighted and gadolinium-enhanced T1-weighted images in the assessment of such invasion and found that considering the patient's menopausal status could improve the accuracy of staging.
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MATERIALS AND METHODS
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From May 1993 to June 1997, 46 consecutive patients with primary untreated endometrial carcinoma were retrospectively evaluated. All patients were referred to our department for MR imaging after histologic diagnosis on the basis of findings at fractional dilation and curettage. The patients were 26–74 years of age (mean, 46 years). Twenty-five women were premenopausal, and 21 were postmenopausal.
The mean interval between curettage and MR imaging was 10 days (range, 1–25 days). The extent of myometrial invasion was confirmed at surgery within 1 week after MR imaging. MR imaging was performed with a 1.5-T superconducting unit (Signa Advantage, GE Medical Systems, Milwaukee, Wis, or Magnetom Vision Plus, Siemens, Erlangen, Germany) and a body coil. T1-weighted imaging was performed with sequences of 400–600/11–19 (repetition time msec/echo time msec) in all 46 patients, T2-weighted imaging with sequences of 2,000–2,200/80–90 in 22 patients, and fast spin-echo imaging with sequences of 3,000–3,200/85–99 in 24 patients in the axial and sagittal planes. Other parameters included a field of view of 24–26 cm for the Signa unit and 188 x 250 mm for the Magnetom unit, two signals acquired, an acquisition matrix of 256 x 192 for the Signa unit and 242 x 512 for the Magnetom unit, 5-mm section thickness and 2.5-mm intersection gap, and an echo train length of eight. Immediately after bolus injection of gadopentetate dimeglumine (0.1 mmol/ kg) (Magnevist; Schering, Berlin, Germany), T1-weighted images were obtained in the axial and sagittal planes.
Working together, two radiologists (E.J.L., J.Y.B.) retrospectively reviewed the images for each patient without knowledge of the histopathologic results. Staging was performed by means of consensus and was based on each patient's T2-weighted images and gadolinium-enhanced T1-weighted images, which were examined separately. At the time of staging, the patient's menopausal status was not known. After staging, the patients were classified as premenopausal (n = 25) or postmenopausal (n = 21). The premenopausal group included 10 patients with stage Ia disease, 14 with stage Ib disease, and one with stage Ic disease. The postmenopausal group included three patients with stage Ia disease, 11 with stage Ib disease, and seven with stage Ic disease.
For staging early endometrial carcinoma with MR images, we basically followed the surgical staging classification of the International Federation of Gynecologists and Obstetricians. As in this classification, we classified early endometrial carcinoma into three stages depending on the depth of invasion observed on MR images: stage Ia (absent; tumor limited to the endometrium with intact junctional zone), stage Ib (superficial; involvement of <50% of the myometrium and disruption or discontinuity of the junctional zone), and stage Ic (involvement of 
50% of the myometrium). When the junctional zone was not visible (ie, there was a smooth interface between the endometrium and the myometrium), the tumor was considered noninvasive. An irregular interface between the endometrium and the myometrium was regarded as myometrial invasion.
The results of staging with T2-weighted images and gadolinium-enhanced T1-weighted images were correlated with the results of histopathologic staging in the combined, premenopausal, and postmenopausal groups by means of the Kendall 
b test. The staging accuracy of each MR imaging technique was also determined for all three groups. In addition, the overall staging accuracy when only T2-weighted imaging was used in the premenopausal group and only gadolinium-enhanced T1-weighted imaging was used in the postmenopausal group (menopausal status–dependent staging) was determined. The Fisher exact test was used to analyze the statistical significance of differences in staging accuracy between T2-weighted and gadolinium-enhanced T1-weighted imaging in the pre- and postmenopausal groups. The 
2 test was used to compare the accuracies of staging with both MR imaging techniques and staging according to menopausal status in all patients.
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RESULTS
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When T2-weighted and gadolinium-enhanced T1-weighted images were used for staging without respect to menopausal status, the staging accuracy was 59% (27 of 46) for T2-weighted images and 61% (28 of 46) for gadolinium-enhanced T1-weighted images (Table 1, Fig 1). When T2-weighted images were used selectively in the premenopausal group, the staging accuracy was increased to 80% (20 of 25). In contrast, gadolinium-enhanced T1-weighted imaging had a staging accuracy of only 44% (11 of 25) in this group (Table 2, Figs 1–3). Conversely,
in the postmenopausal group, gadolinium-enhanced T1-weighted imaging had a staging accuracy of 81% (17 of 21) versus 33% (seven of 21) for T2-weighted imaging (Table 3; Figs 1, 4–6). Therefore, staging with MR imaging became more accurate when T2-weighted imaging was used preferentially in the premenopausal group and gadolinium-enhanced T1-weighted imaging was used preferentially in the postmeno-pausal group (P < .001 [Fisher exact test]) (Fig 1).
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TABLE 1. Results of Staging with T2-weighted Imaging versus Gadolinium-enhanced T1-weighted Imaging in All Patients (n = 46)
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Figure 1. Comparison of staging accuracies for T2-weighted imaging (T2WI), gadolinium-enhanced T1-weighted imaging (Gd-T1WI), and menopausal status-dependent MR staging (MSDMS). * and ** = significantly different (P < .001 [Fisher exact test]). *** = significantly different (P < .05 [2 test]).
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TABLE 2. Results of Staging with T2-weighted Imaging versus Gadolinium-enhanced T1-weighted Imaging in Premenopausal Patients (n = 25)
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Figure 2a. Stage Ib endometrial carcinoma in a 26-year-old premenopausal woman. (a) Axial T2-weighted MR image (3,000/91) shows a lobulated, polypoid, isointense mass in the endometrial cavity (arrowheads) with adjacent junctional zone disruption (arrow), findings that correctly suggest stage Ib disease. (b) Axial gadolinium-enhanced T1-weighted MR image (400/11) shows an irregular endometrial mass (arrow) with no evidence of junctional zone disruption or myometrial invasion, findings that incorrectly suggest stage Ia disease.
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Figure 2b. Stage Ib endometrial carcinoma in a 26-year-old premenopausal woman. (a) Axial T2-weighted MR image (3,000/91) shows a lobulated, polypoid, isointense mass in the endometrial cavity (arrowheads) with adjacent junctional zone disruption (arrow), findings that correctly suggest stage Ib disease. (b) Axial gadolinium-enhanced T1-weighted MR image (400/11) shows an irregular endometrial mass (arrow) with no evidence of junctional zone disruption or myometrial invasion, findings that incorrectly suggest stage Ia disease.
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Figure 3a. Stage Ib endometrial carcinoma in a 40-year-old premenopausal woman. (a) Sagittal T2-weighted MR image (3,200/85) reveals a lobulated, polypoid, hypointense mass that widens the endometrial cavity (arrow). The junctional zone is not demonstrated, and irregularity is identified between the mass and myometrium. The extent of myometrial invasion was assessed as less than 50%, and the tumor was correctly classified as stage Ib. (b) Sagittal gadolinium-enhanced T1-weighted MR image (417/11) shows a hypointense mass confined to the endometrial cavity (arrow), findings that incorrectly suggest stage Ia disease.
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Figure 3b. Stage Ib endometrial carcinoma in a 40-year-old premenopausal woman. (a) Sagittal T2-weighted MR image (3,200/85) reveals a lobulated, polypoid, hypointense mass that widens the endometrial cavity (arrow). The junctional zone is not demonstrated, and irregularity is identified between the mass and myometrium. The extent of myometrial invasion was assessed as less than 50%, and the tumor was correctly classified as stage Ib. (b) Sagittal gadolinium-enhanced T1-weighted MR image (417/11) shows a hypointense mass confined to the endometrial cavity (arrow), findings that incorrectly suggest stage Ia disease.
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TABLE 3. Results of Staging with T2-weighted Imaging versus Gadolinium-enhanced T1-weighted Imaging in Postmenopausal Patients (n = 21)
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Figure 4a. Stage Ib endometrial carcinoma in a 54-year-old postmenopausal woman. (a) Sagittal T2-weighted MR image (3,000/85) shows a lobulated, polypoid mass (arrow) invading the myometrium to more than half of its depth, findings that incorrectly indicate stage Ic disease. (b) Sagittal gadolinium-enhanced T1-weighted MR image (600/11) shows an ovoid, hypointense mass in the endometrial cavity (arrow) and some irregularity at the interface between the mass and the inner surface of the myometrium, findings that correctly suggest stage Ib disease.
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Figure 4b. Stage Ib endometrial carcinoma in a 54-year-old postmenopausal woman. (a) Sagittal T2-weighted MR image (3,000/85) shows a lobulated, polypoid mass (arrow) invading the myometrium to more than half of its depth, findings that incorrectly indicate stage Ic disease. (b) Sagittal gadolinium-enhanced T1-weighted MR image (600/11) shows an ovoid, hypointense mass in the endometrial cavity (arrow) and some irregularity at the interface between the mass and the inner surface of the myometrium, findings that correctly suggest stage Ib disease.
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Figure 5a. Stage Ib endometrial carcinoma in a 57-year-old postmenopausal woman. (a) Sagittal T2-weighted MR image (3,000/85) shows no definite endometrial mass, a finding that incorrectly suggests stage Ia disease. (b) Sagittal gadolinium-enhanced T1-weighted MR image (450/11) shows a discrete hypointense mass (arrow) with invasion of the myometrium to less than half of its depth, findings that correctly suggest stage Ib disease. The histopathologic result corresponded to that of gadolinium-enhanced T1-weighted imaging.
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Figure 5b. Stage Ib endometrial carcinoma in a 57-year-old postmenopausal woman. (a) Sagittal T2-weighted MR image (3,000/85) shows no definite endometrial mass, a finding that incorrectly suggests stage Ia disease. (b) Sagittal gadolinium-enhanced T1-weighted MR image (450/11) shows a discrete hypointense mass (arrow) with invasion of the myometrium to less than half of its depth, findings that correctly suggest stage Ib disease. The histopathologic result corresponded to that of gadolinium-enhanced T1-weighted imaging.
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Figure 6a. Stage Ib endometrial carcinoma in a 60-year-old postmenopausal woman. (a) Sagittal T2-weighted MR image (3,200/99) shows an indistinct junctional zone. There is a slightly hyperintense lesion (arrowheads) in the posterior part of the endometrium with possible focal myometrial invasion (arrow). (b) Sagittal gadolinium-enhanced T1-weighted MR image (600/14) shows a discrete hypointense mass with some marginal irregularity (arrow), which is better demonstrated than on the T2-weighted image (a).
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Figure 6b. Stage Ib endometrial carcinoma in a 60-year-old postmenopausal woman. (a) Sagittal T2-weighted MR image (3,200/99) shows an indistinct junctional zone. There is a slightly hyperintense lesion (arrowheads) in the posterior part of the endometrium with possible focal myometrial invasion (arrow). (b) Sagittal gadolinium-enhanced T1-weighted MR image (600/14) shows a discrete hypointense mass with some marginal irregularity (arrow), which is better demonstrated than on the T2-weighted image (a).
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Stage Ib disease tended to be understaged when gadolinium-enhanced T1-weighted imaging was used in the premenopausal patients (Table 2) and overstaged when T2-weighted imaging was used in the postmenopausal patients (Table 3). The overall accuracy of staging with MR imaging improved to 80% when menopausal status was taken into consideration. (The 80% indicates a ratio of 37:46, where 37 is the number of cases accurately staged with T2-weighted imaging in the premenopausal group and with gadolinium-enhanced T1-weighted imaging in the postmenopausal group and 46 is the total number of patients.) This accuracy was significantly improved compared with the accuracies of 59% (27 of 46) for T2-weighted imaging and 61% (28 of 46) for gadolinium-enhanced T1-weighted imaging used without respect to menopausal status (P < .05 [2 test]) (Fig 1).
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DISCUSSION
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Staging of Early Endometrial Carcinoma on the Basis of Menopausal Status
The depth of myometrial invasion in endometrial carcinoma is an important prognostic factor (6–13). Previous reports concluded that poor contrast between the tumor and the myometrium on T2-weighted images makes it difficult to evaluate myometrial invasion accurately and that dynamic and contrast material–enhanced MR images are therefore superior to T2-weighted images for this evaluation (6–8). We thought that these results might be biased because most patients in those studies were postmenopausal. Unfortunately, dynamic gadolinium-enhanced MR images were not available to us at the time of our retrospective study. It is still unclear whether the staging accuracy of dynamic gadolinium-enhanced MR imaging is also affected by the patient's menopausal status.
Tumors are diagnosed as confined to the endometrium when the junctional zone appears intact. Myometrial invasion can be diagnosed when the junctional zone is disrupted. When the junctional zone is indistinct, a smooth interface between the endometrium and myometrium is considered to represent intact myometrium. However, irregularity of the interface suggests that the tumor has invaded the myometrium (6–13).
In postmenopausal women, the junctional zone is usually poorly demonstrated on T2-weighted images, and there is no difference between the appearance of this zone on T2-weighted images and on gadolinium-enhanced T1-weighted images (6–8). In premenopausal women, however, the junctional zone is usually better demonstrated on T2-weighted images. In our 25 premenopausal patients, staging was more accurate with T2-weighted images, especially the distinction between stage Ia and Ib disease. In contrast to the previous reports that staging is more accurate with gadolinium-enhanced T1-weighted imaging (6–8), we found that T2-weighted imaging was more useful in the premenopausal group (Figs 2, 3) because it better demonstrated the low-signal-intensity junctional zone and disruption or irregularity of this zone. However, because the junctional zone changes histologically during menopause, gadolinium-enhanced T1-weighted imaging was more useful in detecting tumor and evaluating myometrial invasion in postmenopausal patients (Figs 4–6). Therefore, the MR imaging technique used for staging should depend on the patient's menopausal status.
Some cases of stage Ib disease were over-staged when staging was performed with T2-weighted imaging in postmenopausal patients, and some cases were understaged when staging was performed with gadolinium-enhanced T1-weighted imaging in premenopausal patients. Tumors isointense to the myometrium and poor demonstration of the junctional zone on T2-weighted images were the main causes of over-staging, especially in some postmenopausal patients with stage Ib disease, whereas an obscured junctional zone after gadolinium enhancement was the reason for understaging in some premenopausal patients with stage Ib tumors.
Pitfalls in Staging Endometrial Cancer with MR Imaging
We found several pitfalls in assessing the depth of myometrial invasion in stage I endometrial carcinoma: nonvisualization of a mass after curettage, a bulky polypoid tumor, a small uterus, a well-enhancing junctional zone, adenomyosis, leiomyoma, and retroversion of the uterus. Some of these findings are consistent with those previously reported (14). In our study, all MR images were obtained after uterine curettage. MR images obtained before uterine curettage were unfortunately not available for comparison, but we believe that the mass may have been removed at uterine curettage in some cases.
In 10 cases, incorrect differentiation between stage Ia and Ib disease occurred with at least one MR imaging technique because the tumor was not visualized or was too small. In five patients, a bulky polypoid tumor distended the endometrial cavity, thus attenuating the myometrium. This attenuation caused overstaging with at least one MR imaging technique. One of these five patients had a small uterus (<5 cm in longitudinal diameter) and demonstrated marked thinning of the myometrium by a large, polypoid endometrial mass. In some cases with junctional zone involvement, it was difficult to assess the depth of invasion on gadolinium-enhanced T1-weighted images because the junctional zone was enhanced as well as the myometrium and thus could not be distinguished. T2-weighted imaging was more useful in evaluating tumor extension into the junctional zone (Fig 7).
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Figure 7a. Stage Ib endometrial carcinoma in a 35-year-old premenopausal woman. (a) Sagittal T2-weighted MR image (2,000/90) shows focal disruption of the junctional zone (arrow) at the lower anterior wall. The well-defined junctional zone shows the exact extent of disease. (b) Sagittal gadolinium-enhanced T1-weighted MR image (500/11) shows an irregular interface between the myometrium and the endometrial mass. Focal deep invasion of the myometrium (arrow) indicates stage Ic disease. The histopathologic result was consistent with the stage at T2-weighted imaging. Gadolinium enhancement obliterated the distinction between the junctional zone and the outer myometrium and thus led to overstaging.
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Figure 7b. Stage Ib endometrial carcinoma in a 35-year-old premenopausal woman. (a) Sagittal T2-weighted MR image (2,000/90) shows focal disruption of the junctional zone (arrow) at the lower anterior wall. The well-defined junctional zone shows the exact extent of disease. (b) Sagittal gadolinium-enhanced T1-weighted MR image (500/11) shows an irregular interface between the myometrium and the endometrial mass. Focal deep invasion of the myometrium (arrow) indicates stage Ic disease. The histopathologic result was consistent with the stage at T2-weighted imaging. Gadolinium enhancement obliterated the distinction between the junctional zone and the outer myometrium and thus led to overstaging.
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In seven cases with associated adenomyosis, the myometrium had heterogeneous signal intensity on T2-weighted images, an appearance that led to misstaging. Manifestations of adenomyosis at MR imaging are uterine enlargement, a poorly defined hypointense area, heterogeneous signal intensity of a hypertrophic myometrium with small hyperintense foci on T2-weighted images, and junctional zone widening (15). These findings make it difficult to determine the tumor margin. In these cases, gadolinium-enhanced T1-weighted images were preferable to T2-weighted images for accurate staging (Fig 8). In two of five cases of leiomyoma, an intramural mass at the junctional zone distorted the zonal anatomy and caused misstag-ing. A retroverted uterus was seen in two cases and led to overstaging on axial images. In these cases, the sagittal images enabled the tangential depth of the myometrial invasion to be evaluated accurately.
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Figure 8a. Stage Ic endometrial carcinoma in a 61-year-old postmenopausal woman. (a) Axial T2-weighted MR image (3,000/85) shows a slightly hyperintense mass in the endometrial cavity (black arrowheads). The junctional zone is disrupted at the anterior aspect (white arrowheads), but the tumor margin is indistinct. An ill-defined hypointense area is noted at the anterior wall of the uterus (arrows). At histopathologic analysis, this area proved to be underlying adenomyosis. (b) Axial gadolinium-enhanced T1-weighted MR image (500/11) shows adenomyosis (arrows), which is better differentiated from the endometrial carcinoma (arrowheads) than on the T2-weighted image (a).
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Figure 8b. Stage Ic endometrial carcinoma in a 61-year-old postmenopausal woman. (a) Axial T2-weighted MR image (3,000/85) shows a slightly hyperintense mass in the endometrial cavity (black arrowheads). The junctional zone is disrupted at the anterior aspect (white arrowheads), but the tumor margin is indistinct. An ill-defined hypointense area is noted at the anterior wall of the uterus (arrows). At histopathologic analysis, this area proved to be underlying adenomyosis. (b) Axial gadolinium-enhanced T1-weighted MR image (500/11) shows adenomyosis (arrows), which is better differentiated from the endometrial carcinoma (arrowheads) than on the T2-weighted image (a).
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One limitation of our study was that there was only one case of stage Ic endometrial carcinoma in a premenopausal patient. Further evaluations should include more such cases.
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CONCLUSIONS
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MR imaging is useful in assessing the depth of myometrial invasion in patients with early-stage endometrial carcinoma. In previous studies, gadolinium-enhanced T1-weighted imaging was found to be superior to T2-weighted imaging for accurate staging. However, we found that staging with MR imaging can be more accurate when T2-weighted imaging is used in premenopausal patients and gadolinium-enhanced T1-weighted imaging is used in postmenopausal patients. Thus, consideration of menopausal status and selection of the proper pulse sequence can be important for accurate staging with MR imaging and proper surgical and therapeutic planning. Choosing the MR imaging technique according to the patient's menopausal status can improve the accuracy of staging with MR imaging in early endometrial carcinoma.
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Footnotes
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See the commentary by Outwater
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Related Article
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Invited Commentary
- Eric K. Outwater
RadioGraphics 1999 19: 946-947.
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Abstract
INTRODUCTION
