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1 Department of Radiology, Kumamoto University School of Medicine, 1-1-1, Honjo,
Kumamoto, Kumamoto 860-8556, Japan.
2 Department of Obstetrics and Gynecology, Kumamoto University School of
Medicine, Kumamoto 860-8556, Japan.
3 Department of Radiology, Kinki University School of Medicine, 377-2,
Ohnohigashi Hazayama, Osaka 589-8511, Japan.
Received April 2, 2003;
accepted after revision August 25, 2003.
Presented at the 2003 annual meeting of the American Roentgen Ray Society,
San Diego, CA.
Abstract
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MATERIALS AND METHODS. We retrospectively reviewed the MRIs of 11 patients who had a total of 12 lesions of endometrial carcinoma within adenomyosis. T2-weighted and contrast-enhanced dynamic T1-weighted images were compared with the histologic findings separately. We assessed the extent of myometrial invasion by endometrial carcinomas. The depth of myometrial invasion seen on MRI was classified as stage S (superficial invasion), stage D (deep invasion), or undetectable. The staging accuracies of each sequence were assessed. The tumor–myometrium contrast-to-noise ratios were calculated for each sequence.
RESULTS. The histologic specimens revealed that myometrial invasion was deep in seven of 12 lesions and superficial in five. On T2-weighted images the depth of invasion was underestimated in two lesions and impossible to determine in five lesions. On dynamic T1-weighted images the depth of invasion was overestimated in one lesion and underestimated in one lesion. The staging accuracy on dynamic T1-weighted images (83%) was significantly higher than that on T2-weighted images (42%). The contrast-to-noise ratio was significantly higher on dynamic T1-weighted studies during the early phase (mean ± SD, 2.68 ± 0.94) than it was on T2-weighted studies (1.74 ± 1.05) and during the delayed phase (2.01 ± 0.86).
CONCLUSION. When adenomyosis coexists with endometrial cancer at the same site on T2-weighted images, contrast-enhanced dynamic T1-weighted imaging improves the accuracy of staging.
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MRI has been used to evaluate myometrial invasion. Previous studies have suggested that MRI gives results with relatively high accuracy and is useful for evaluating myometrial invasion by endometrial carcinoma [4–16].
Endometrial cancer sometimes coexists with adenomyosis [17–21] but rarely arises from adenomyosis itself. Manifestations of adenomyosis on T2-weighted images are uterine enlargement, a poorly defined hypointense area, heterogeneous signal intensity of a hypertrophic myometrium with small hyperintense foci, and an obscure junctional zone [22]. These findings may make it difficult to determine the margin of endometrial cancer and lead to errors in staging [23]. However, assessment of myometrial invasion of endometrial cancer within adenomyosis has been the subject of only a few studies [24, 25].
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MRI Technique
MRI was performed with a 1.5-T superconductive unit (Symphony or Magnetom
Vision, Siemens, Erlangen, Germany) using a phased array coil. Spin-echo
T1-weighted images (TR/TE, 634/12; matrix, 256 x 256) and turbo
spin-echo T2-weighted images (3,700/120; matrix, 300 x 512) were
obtained. Imaging was performed in the sagittal and axial planes with a 5-mm
slice thickness, 1-mm interslice gap, and 20-cm field of view. The dynamic
study, consisting of serial imaging with turbo spin-echo T1-weighted sequence,
was performed with parameters of 270/12; flip angle, 90°; and matrix, 168
x 256. Images were also obtained in the sagittal plane with a 5-mm slice
thickness, 1-mm interslice gap, and 20-cm field of view before and after a
bolus injection of contrast medium. Contrast-enhanced dynamic turbo spin-echo
T1-weighted images were obtained by a multislice technique in each series,
with an acquisition time of approximately 1 min.
Gadopentetate dimeglumine (Magnevist [0.1 mmol/kg], Schering, Berlin, Germany) was administered by rapid manual injection over approximately 10 sec through an angiocatheter into an antecubital vein. The beginning of contrast medium administration was taken as the zero point. Contrast-enhanced dynamic imaging was performed by obtaining early phase images (60 sec after starting the injection) followed by delayed phase images (120 or 240 sec after starting the injection).
Image Interpretation
All MRIs were retrospectively reviewed by two radiologists who did not know
the pathologic results. Neither reviewer was involved in the image
interpretation of the cases before beginning this study. Reviewers visually
assessed the appearance of adenomyosis on T2-weighted images and the
appearance of myometrial enhancement on dynamic MRIs for each patient. Next,
they assessed the degree of myometrial invasion on T2-weighted images and
dynamic T1-weighted images separately for each patient. The assessments of the
MRI appearance and staging were performed by consensus.
The diagnosis of adenomyosis was based on MRI when diffuse or focal thickening of the junctional zone measured 12 mm or more. Secondary findings such as poor definition of borders or high-signal-intensity foci were used to diagnose adenomyosis in patients with a maximal junctional zone thickness of 8–12 mm. The depth of myometrial invasion was classified on MRI as stage S (superficial invasion: tumor is limited to endometrium or invades 50% or less of the myometrium), stage D (deep invasion: tumor invades more than 50% of the endometrium), or undetectable (the extent of myometrial invasion could not be determined).
The MRI criteria for classifying the depth of myometrial invasion by endometrial carcinoma were as follows: For stage S, the junctional zone on T2-weighted images, if present, appeared to be intact or have segmental interruption. When no junctional zone was visible, the presence of a smooth endometrium–myometrium interface was considered an indicator of noninvasive cancer. On contrast-enhanced MRIs, the inner surface of the enhanced myometrium was smooth, or abnormal intensity of the tumor appeared to expand into the inner half of the myometrium. For stage D, the tumor signal intensity appeared to expand into the outer half of the myometrium and residual myometrium was thin or interrupted.
The results of MRI staging were compared with the results of histopathologic staging (Tables 1 and 2). The accuracies of MRI staging were assessed. The McNemar test was used to analyze the statistical significance of differences in assessing the staging accuracies of MRI. Instances in which myometrial invasion was impossible to determine were counted as inaccurate for MRI staging, and the reasons for the staging errors were assessed.
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One radiologist assessed the tumor–myometrium contrast-to-noise ratio (CNR) quantitatively. One radiologist performed operator-defined region-of-interest (ROI) measurements of the mean signal intensity of the tumor, the surrounding myometrium, and the background noise on T2-weighted images and on contrast-enhanced dynamic MRIs during the early and the delayed phases. Circular or oval ROIs were drawn to include the largest area in the ROI. The SDs of background noise were measured on the images along the phase-encoding direction in space outside the body. ROIs were drawn twice in each place, and mean values were calculated. All ROIs were obtained between 5 and 10 cm from the coil.
The CNR between the tumor and the surrounding myometrium was obtained as
follows:
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MRI Appearance
On T2-weighted images, all patients showed MRI findings matching the MRI
criteria for adenomyosis. The predominant lesion of adenomyosis detected on
MRI consisted of a low-signal-intensity area that gave the appearances of
focal or diffuse widening of the junctional zone and a poorly defined
decreased-signal-intensity mass that replaced the myometrium. Tumor signal
intensity ranged from slight hyperintensity to hypointensity when compared
with the moderate signal intensity of the myometrium.
On contrast-enhanced dynamic T1-weighted images, the enhancement findings of myometrium were as follows: The inner layer of myometrium showed marked enhancement during the early phase in all patients except one. The whole myometrium was enhanced during the delayed phase in all patients. Low-signal-intensity foci were frequently seen, and the enhancement of such foci was gradual. A tumor was seen as a slowly and slightly enhanced lesion that contrasted well with the rapidly and strongly enhanced myometrium.
MRI Staging
The depth of invasion was underestimated in two lesions and impossible to
estimate in five lesions on T2-weighted images. The depth of invasion was
overestimated in one lesion and underestimated in one lesion on
contrast-enhanced MRI. The results of assessment of myometrial invasion with
T2-weighted images, contrast-enhanced dynamic T1-weighted images, and
histologic findings are presented in Tables
1 and
2. The staging accuracy with
MRI was 42% (5/12) for T2-weighted images and 83% (10/12) for
contrast-enhanced dynamic MRIs. The sensitivity and the specificity of
T2-weighted images in differentiating deep myometrial invasion from
superficial invasion were 40% and 43%, respectively; the corresponding values
of contrast-enhanced MRI were 80% and 86%, respectively. The staging accuracy
for contrast-enhanced dynamic T1-weighted images was higher than that for
T2-weighted images. The difference in staging accuracy with MRI was
statistically significant (McNemar test, p < 0.05). Myometrial
invasion by the tumor tended to be underestimated or indistinguishable from
myometrium on T2-weighted images. Poor contrast between the tumor and the
myometrium caused by the associated adenomyosis led to misinterpretation on
all imaging techniques.
CNR Analysis
On contrast-enhanced MRIs during the early phase, the
tumor–myometrium CNR was 2.68 ± 0.94 (mean ± SD). During
the delayed phase, the tumor–myometrium CNR was 2.01 ± 0.86. On
T2-weighted images, the tumor–myometrium CNR was 1.74 ± 1.05.
When CNRs were compared for images obtained with each sequence,
contrast-enhanced T1-weighted images obtained during the early phase had a
higher CNR than did T2-weighted or dynamic contrast-enhanced T1-weighted
images obtained during the delayed phase. The difference in
tumor–myometrium contrast was statistically significant (paired
Student's t test, p < 0.05).
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Adenomyosis is a common disease characterized by the presence of heterotopic endometrial glands and stroma in the myometrium with adjacent smooth-muscle hyperplasia; its incidence is 8.1–16.7% of the at risk population [17, 18, 24, 26]. Adenomyosis was found in association with endometrial carcinoma in 19.4% of patients in a series reported by Greenwood [18]. The histopathologic features of adenomyosis are varied and contribute to its imaging appearance [24]. Coexistence of adenomyosis and endometrial carcinoma at the same site frequently makes the tumor margin indistinguishable, and caution must be taken not to misinterpret findings. Previous reports concluded that poor contrast between the tumor and the myometrium on T2-weighted images made it difficult to evaluate myometrial invasion accurately, which therefore made contrast-enhanced MRIs superior to T2-weighted images for this evaluation [4–6, 12].
To the best of our knowledge, the enhancement pattern of a uterus with adenomyosis on contrast-enhanced dynamic MRIs has not been reported. In our study, the inner layer of myometrium showed marked enhancement during the early phase and the whole myometrium was enhanced during the delayed phase in all cases except one. Focal low-signal-intensity areas were seen frequently during the early phase, and the enhancement of the focal low-signal-intensity areas was gradual and slightly less intense than the enhancement of surrounding myometrium during the delayed phase. The mechanism of this enhancement pattern is unclear. We hypothesize that the area of junctional zone enhancement corresponds to this vascularized inner layer, and the accompanying smooth-muscle hyperplasia corresponds to the focal low-signal-intensity area. Contrast-enhanced MRI features during the early phase were useful for assessing myometrial invasion because we frequently saw marked enhancement of the inner layer of myometrium, and contrast-enhanced dynamic MRI showed the tumor with significantly better contrast during the early phase than T2-weighted images did. Contrast-enhanced dynamic MRIs were superior to T2-weighted images in staging accuracy in cases of endometrial carcinoma with adenomyosis. Contrast-enhanced dynamic T1-weighted images may be preferable for the preoperative assessment of myometrial invasion in such cases. Focal abnormal signals or irregular enhancement can be mistaken for tumor invasion and result in staging errors.
This study has several limitations. First, contrast-enhanced dynamic MRI could be performed only in a few imaging planes with the 2D multislice technique used in this study. However, contiguous thinner section images could be obtained by means of 3D imaging acquisitions with better signal-to-noise ratios. Second, the spatial resolution on dynamic MRI is inferior to that on conventional spin-echo sequences. Third, our study group was small, and additional studies are needed to assess the role of contrast-enhanced MRI more definitively.
In summary, diagnosis of myometrial invasion in endometrial carcinoma in adenomyosis appears to be less accurate on T2-weighted images. Contrast-enhanced dynamic MRI improves the accuracy of MRI staging and aids in proper surgical and therapeutic planning.
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