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DOI:10.2214/AJR.07.2380
AJR 2008; 190:489-495
© American Roentgen Ray Society


Original Research

3-T MRI in the Preoperative Evaluation of Depth of Myometrial Infiltration in Endometrial Cancer

Pietro Torricelli1, Sonia Ferraresi1, Federica Fiocchi1, Guido Ligabue1, Valerio M. Jasonni2, Ilaria Di Monte2 and Francesco Rivasi3

1 Department of Radiology, University of Modena and Reggio-Emilia, Policlinico, Via del Pozzo 71, 41100 Modena, Italy.
2 Department of Gynecology, University of Modena and Reggio-Emilia, Modena, Italy.
3 Department of Pathology, University of Modena and Reggio-Emilia, Modena, Italy.

Received April 6, 2007; accepted after revision September 5, 2007.

 
Address correspondence to P. Torricelli (torricelli.pietro{at}unimore.it).


Abstract
Top
Abstract
Introduction
subjects and Methods
Results
Discussion
References
 
OBJECTIVE. The objective of our study was to evaluate the diagnostic accuracy of 3-T MRI in determining the depth of myometrial infiltration in patients with endometrial cancer.

SUBJECTS AND METHODS. Fifty-two patients (43 postmenopausal) with histopathologically proven endometrial carcinoma underwent preoperative 3-T MRI. The following sequences were performed: axial T1 fast spin-echo (FSE); axial, parasagittal, and paracoronal T2 FSE; paracoronal 3D T1 inversion recovery gradient-echo after contrast administration; and parasagittal fat-suppressed T1 FSE. All patients underwent a hysterectomy. The MRI findings were compared with histopathology results. The quantity and degree of artifacts were evaluated.

RESULTS. MRI performed on a 3-T unit was in agreement with histopathology in assessing the depth of invasion in 86.4% (44/52) of the patients with a mean sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and accuracy of 83.5%, 93.9%, 77.8%, 92.2%, and 89.7%, respectively. Performance values were also assessed for single stages of myometrial infiltration. For the detection of an intramucosal lesion (MRI, 12/52; histopathology, 6/52), sensitivity was 100%; specificity, 86.9%; PPV, 50%; NPV, 100%; and accuracy, 88.5%. For the detection of myometrial infiltration that was less than 50% (MRI, 12/52; histopathology, 16/52), sensitivity was 62.5%; specificity, 94.4%; PPV, 83.3%; NPV, 85%; and accuracy, 84.6%. For the detection of myometrial infiltration that was greater than 50% (MRI, 28/52; histopathology, 30/52), sensitivity was 93.3%; specificity, 100%; PPV, 100%; NPV, 91.7%; and accuracy, 96.2%. The following artifacts were found: abdominal wall movement, nine patients (not affecting image quality); peristalsis, 16 patients (two deeply affecting, one affecting, and 13 scarcely affecting); magnetic susceptibility artifact, four patients (not affecting); chemical shift, 20 patients (four scarcely affecting and 16 not affecting); and dielectric effect, six patients (four deeply affecting and two affecting).

CONCLUSION. In evaluating the depth of myometrial infiltration in patients with endometrial cancer, 3-T MRI showed high diagnostic accuracy—equivalent to that of 1.5-T MRI reported in the literature. Artifacts did not significantly affect image quality.

Keywords: 3-T MRI • endometrial carcinoma • high-field-strength MRI • myometrial invasion • staging • women's imaging


Introduction
Top
Abstract
Introduction
subjects and Methods
Results
Discussion
References
 
MRI is currently considered the most accurate imaging technique for staging endometrial cancer—in particular, for assessing the depth of myometrial infiltration, which is crucial from both a prognostic and a therapeutic planning standpoint [19]. On one hand, the recent introduction of faster sequences after gadolinium injection has further improved the diagnostic performance of MRI, with an overall staging accuracy that ranges from 83% to 92% [1014]; on the other hand, some authors state that T2-weighted imaging is more accurate than contrast-enhanced imaging, especially in the premenopausal state [10]. For abdominal and pelvic evaluation, 1.5-T MRI has been widely used because the signal-to-noise ratio (SNR) allows a higher temporal and spatial resolution [15]. MRI at 3-T MRI offers advantages over 1.5-T MRI: an almost doubled SNR, higher spectral definition, and better blood oxygenation level–dependent contrast; therefore, 3-T MRI has established applications in the neuroradiologic field [16, 17]. However, the advantages of higher magnetic fields cannot be directly transferred to body applications because there are numerous restrictions, including tissue radiofrequency deposition, an increase in T1 relaxation time, reduction in T2 relaxation time, insufficient penetration of radiofrequency, greater magnetic susceptibility artifacts, and chemical shift artifacts [1820]. The use of 3-T MRI for abdominal and pelvic studies is therefore somewhat scarce and only a few groups have evaluated its pelvic applications [2124]. In particular, reviewing the current literature, we found no reports that deal with the staging accuracy of 3-T MRI in patients with endometrial cancer.

The aim of this study was to evaluate the diagnostic accuracy and the limits of 3-T MRI in determining the depth of myometrial infiltration in patients with endometrial cancer.


subjects and Methods
Top
Abstract
Introduction
subjects and Methods
Results
Discussion
References
 
Between February 2005 and September 2006, 62 patients with endometrial adenocarcinoma diagnosed by endometrial biopsy were evaluated. The mean time interval between biopsy and MRI was 15 days (range, 12–18 days). Two patients were excluded because the definitive histopathology was not adenocarcinoma (carcinosarcoma). Six patients at high surgical risk of complications did not undergo surgery. Two patients would not consent to be included in the study. The final population enrolled was 52 patients (mean age, 63.1 ± 14.6 years), 82.7% of whom were postmenopausal.

All patients gave written informed consent to undergo the study protocol, and the study was approved by our institutional review board. All underwent 3-T MRI (Intera, Philips Medical Systems) using a six-channel phased-array coil (Sense Cardio, Philips). Twenty milligrams of butyl-scopolamine (Buscopan, Schering) was IV administered to all patients except when contraindicated before the examination to prevent peristalsis artifacts. All patients were asked to fast for at least 2 hours before the procedure and to void before the examination to reduce full-bladder compression of the uterus. A respiratory-gating system was applied to minimize breathing movement artifacts. In 51 of the 52 cases, a rest slab was positioned in the anterior part of the abdomen to reduce artifacts due to abdominal wall movements.

MR Sequences
Axial T1-weighted fast spin-echo (FSE) imaging (TR/TE, 574/10) was performed from the renal hila to the pubic symphysis using the following parameters: slice thickness, 5 mm; intersection gap, 1 mm; number of signal averages (NSA), 2; matrix, 256 x 256; field of view (FOV), 20–25 cm, according to patient's body habitus; and voxel size, 0.98 x 0.97 x 5 mm.

Axial, parasagittal, and paracoronal T2-weighted FSE imaging (TR range/TE, 4,299–4,893/100) was performed using the following parameters: slice thickness, 4 mm; intersection gap, 1 mm; NSA, 2; matrix, 512 x 512; FOV, 20–25 cm; and voxel size, 0.98 x 0.98 x 5 mm. The parasagittal scans were obtain parallel to the long uterine axis, whereas the paracoronal scans were obtained orthogonal to the long uterine axis and parallel to the short uterine axis. The axial scans were obtained with fat saturation.

To reduce the specific absorption rate, we combined the use of long-TR sequences, parallel imaging (sensitivity encoding [SENSE]), and a refocusing flip angle.

Paracoronal 3D T1-weighted high-resolution isotropic volume examination (THRIVE) sequences were performed: TR/TE, 6.3/3; flip angle, 10°; slice thickness, 3 mm; intersection gap, over continuous slices; NSA, 1; matrix, 192 x 256; FOV, 20–25 cm; and voxel size, 0.98 x 0.97 x 5 mm. The paracoronal scans were obtained orthogonal to the long uterine axis and parallel to the short uterine axis. This sequence was used for a dynamic contrast-enhanced study for which images were acquired at four different phases relative to the IV injection of contrast agent (0.2 mL/kg of gadoterate dimeglumine [Dotarem, Guerbet]): basal (before gadolinium injection), arterial (30 seconds after injection), venous (60 seconds), and late (120 seconds). Most of the images used for diagnostic assessment were venous phase images.

Parasagittal fat-suppressed T1-weighted FSE imaging (589/10) was performed 180 seconds after gadolinium injection. This sequence was performed when cancer was suspected to have spread beyond the uterine serosa to the parametrial tissue according to previous sequence findings.

Assessment of MR Images
Two radiologists independently assessed the depth of myometrial infiltration by evaluating both the T2-weighted sequences (axial, parasagittal, and paracoronal) and the paracoronal contrast-enhanced 3D T1-weighted inversion recovery sequence, and interobserver variability was reported. In cases of discordance between the two sequences—T2-weighted and 3D T1-weighted after contrast administration—the latter was considered to be the more reliable sequence [1014].

The MRI criteria used to assess the degree of the myometrial invasion on both T2-weighted and contrast-enhanced T1-weighted sequences were described by Frei and Kinkel [25] and are reported in Table 1. MRI assessment of myometrial infiltration was performed according to the surgical–pathologic classification criteria proposed by the International Federation of Gynecology and Obstetrics (FIGO), which classifies stage I endometrial cancer as follows: IA, tumor is restricted to the endometrium without myometrial infiltration; IB, tumor infiltrates less than 50% of the thickness of the myometrium; and IC, tumor infiltrates more than 50% of the myometrium.


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TABLE 1: MRI Criteria for the Assessment of Myometrial Invasion

 

Furthermore, the presence of artifacts on images obtained of each patient was assessed. The influence of the artifacts on the image diagnostic value was graded on a scale of 1–4, as follows: 1 (not affecting image quality), artifacts did not influence diagnostic image quality; 2 (scarcely affecting), artifacts caused minor loss in quality but did not interfere with ability to assess myometrial invasion; 3 (affecting), artifacts caused a significant loss of quality and impaired myometrial invasion assessment; and 4 (deeply affecting), artifacts rendered an image uninterpretable. Images evaluated as grades 3 and 4 were not considered diagnostic. Two radiologists independently assessed the impact of artifacts on image diagnostic value, and interobserver agreement was expressed as a kappa value.

Within 1 month after MRI examination, all patients underwent hysterectomy. The whole surgical specimen was sectioned along the coronal plane orthogonal to the main uterine axis, and histologic macrosections were obtained and routinely stained with H and E. The degree of myometrial infiltration was subsequently quantified according to the FIGO criteria.

A comparative evaluation of MRI findings and histopathologic results was performed. The anatomic macrosections were considered the gold standard.

Statistical Analysis
Sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and diagnostic accuracy of 3-T MRI were calculated (Stata software, Stata Corporation). Furthermore, the impact of artifacts on diagnosis was assessed.

The kappa statistic (Stata, release 9.0, Stata Corporation) was used to estimate interobserver agreement. The thresholds used for interpreting the results were as follows: < 0.0, poor; 0.00–0.20, slight; 0.21–0.40, fair; 0.41–0.60, moderate; 0.61–0.80, substantial; and 0.81–1.00, almost perfect.


Results
Top
Abstract
Introduction
subjects and Methods
Results
Discussion
References
 
Staging Accuracy
Forty-three of the 52 patients evaluated were in a menopausal state, 20 of whom were being treated with hormone replacement therapy. Assessing the uterine zone anatomy in six of 23 patients was difficult, but with integration of the criteria reported in Table 1, a final diagnosis was made on MR images in all patients.

Anatomic evaluation showed intramucosal tumor in six patients (stage pIA) and myometrial infiltration of less than 50% in 16 patients (stage pIB) and greater than 50% in 30 (stage pIC).

MRI evaluation using 3 T depicted 12 cases of intramucosal tumor, 12 cases of myometrial infiltration less than 50% (Figs. 1A, 1B, 1C and 2A, 2B, 2C), and 28 cases of myometrial infiltration greater than 50% (Figs. 3A, 3B, 3C and 4A, 4B).


Figure 1
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Fig. 1A 52-year-old woman with stage IB endometrial carcinoma. Sagittal (A) and coronal (B) fast spin-echo T2-weighted images show huge endometrial tumor that enlarges endometrial cavity. In anteroinferior part of uterus body, junctional zone (arrow) is thinned and not clearly visible. Myometrium is thinned to less than 50% of its thickness. Multiple uterine fibroids are present.

 

Figure 2
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Fig. 1B 52-year-old woman with stage IB endometrial carcinoma. Sagittal (A) and coronal (B) fast spin-echo T2-weighted images show huge endometrial tumor that enlarges endometrial cavity. In anteroinferior part of uterus body, junctional zone (arrow) is thinned and not clearly visible. Myometrium is thinned to less than 50% of its thickness. Multiple uterine fibroids are present.

 

Figure 3
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Fig. 1C 52-year-old woman with stage IB endometrial carcinoma. Paracoronal gadolinium-enhanced T1-weighted image in arterial phase shows subendometrial enhancement line in anteroinferior part is thinned and irregular but is continuous. These findings suggest that myometrial infiltration is less than 50%.

 

Figure 4
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Fig. 2A 56-year-old woman with stage IB endometrial carcinoma. Sagittal fast spin-echo T2-weighted image shows endometrial cavity is occupied by hypointense mass that causes thinning of junctional zone (arrow) in inferior part of uterine body.

 

Figure 5
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Fig. 2B 56-year-old woman with stage IB endometrial carcinoma. Paracoronal gadolinium-enhanced T1-weighted images in arterial (B) and late (C) phases show that subendometrial enhancement line is irregularly enhanced but is continuous. These findings suggest superficial invasion of myometrium.

 

Figure 6
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Fig. 2C 56-year-old woman with stage IB endometrial carcinoma. Paracoronal gadolinium-enhanced T1-weighted images in arterial (B) and late (C) phases show that subendometrial enhancement line is irregularly enhanced but is continuous. These findings suggest superficial invasion of myometrium.

 

Figure 7
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Fig. 3A 59-year-old woman with stage IC endometrial carcinoma. Sagittal fast spin-echo T2-weighted image shows large, lobulated, and hypointense mass completely interrupting junctional zone (arrow) and deeply invading myometrium. Multiple fibroids are also visible. Extent of myometrial invasion was assessed as more than 50%.

 

Figure 8
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Fig. 3B 59-year-old woman with stage IC endometrial carcinoma. Axial gadolinium-enhanced T1-weighted MR images in arterial (B) and late (C) phases confirm hypointense mass has invaded more than 50% of myometrium thickness (arrowhead).

 

Figure 9
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Fig. 3C 59-year-old woman with stage IC endometrial carcinoma. Axial gadolinium-enhanced T1-weighted MR images in arterial (B) and late (C) phases confirm hypointense mass has invaded more than 50% of myometrium thickness (arrowhead).

 

Figure 10
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Fig. 4A 57-year-old woman with stage IC endometrial carcinoma. Sagittal fast spin-echo T2-weighted image shows slightly hyperintense tumor deeply invading myometrium (arrow) in inferior part of uterine body. Junctional zone is not visible. Cervical nabothian cyst is also visible.

 

Figure 11
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Fig. 4B 57-year-old woman with stage IC endometrial carcinoma. Paracoronal gadolinium-enhanced T1-weighted image in late phase shows better than A that transmyometrial infiltration of tumor reaches serosa in anterior part of uterine corpus (arrowhead).

 
MRI at 3 T resulted in understaging six cases of superficial myometrial invasion misinterpreted as intramucosal stage and two cases of deep invasion misinterpreted as superficial invasion. The overall agreement between MRI and pathology was 84.6% (44/52).

Statistical evaluations of 3-T MRI showed an overall sensitivity of 83.5% (95% CI, > 0.748 to < 0.944), specificity of 93.9% (> 0.872 to < 0.974), PPV of 77.8%, and NPV of 92.2%. The overall accuracy was 89.7%.

For single stages of myometrial invasion, the statistical values are summarized in Table 2. The 95% CIs were also calculated by stage for the following data: for an intramucosal lesion, specificity was 86.9% (95% CI, > 0.772 to < 0.967); for myometrial infiltration less than 50%, sensitivity was 62.5% (> 0.388 to < 0.862) and specificity was 94.4% (> 0.870 to < 1.019); for myometrial infiltration greater than 50%, sensitivity was 93.3% (> 0.844 to < 1.023).


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TABLE 2: Statistical Values for Single Stages of Myometrial Infiltration

 

Agreement between the two radiologists was almost perfect ({kappa} = 0.92).

Artifacts
The following artifacts were found and are summarized in Table 3: Abdominal wall movement artifact, peristaltic movements, magnetic susceptibility artifact, chemical shift, and dielectric effects.


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TABLE 3: Kinds and Numbers of Artifacts Seen on 3-T MRI of 52 Cases of Endometrial Cancer

 

Agreement between the two radiologists was almost perfect ({kappa} = 0.85).


Discussion
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Abstract
Introduction
subjects and Methods
Results
Discussion
References
 
The diagnostic impact of 3-T MRI in body applications has not been acknowledged, even though researchers expect that the SNR doubling that can be obtained using 3-T systems may translate into a significant improvement in the clinical performance of MRI [26]. A few authors have evaluated the role of 3-T MRI in imaging the female pelvis. Morakkabati-Spitz et al. [23] compared the quality of images acquired using 1.5-T MRI and 3-T MRI in a group of 19 patients. They concluded that "with regard to image contrast, both qualitative analysis and quantitative analysis revealed comparable image contrast for the 1.5- and 3-T protocols." They also stated that there was no difference between the two systems in tumor diagnosis and staging. However, no case of endometrial cancer was considered in their population. In a more recent study [24], the same group evaluated the diagnostic potential of a new 3-T turbo spin-echo T2-weighted sequence in a population of 23 women with pelvic abnormalities. They concluded that high spatial definition can be obtained using a 3-T scanner with acceptable scanning times. However, cases of endometrial carcinoma were not included in their study.

In our study, a high specificity and PPV were found for 3-T MRI, as correlated with pathologic results, in evaluating the depth of myometrial infiltration. In particular, the high specificity (93.3%) and PPV (100%) obtained in detecting deep myometrial infiltration should be highlighted because, as has been described by others [6, 13, 14], deep (> 50%) myometrial infiltration is linked to lymph node positivity and is one of the most important factors affecting prognosis and therapy.

Eight of the 52 cases were understaged: in three of the eight cases, slight myometrial infiltration was identified only at histopathologic evaluation and was not detectable even when the MR images were reviewed retrospectivvely. In the remaining five cases, understaging was due to poor visualization or a lack of visualization of both the junctional zone in the T2-weighted sequences and the subendometrial enhancement in the contrast-enhanced T1-weighted sequences, likely due to the postmenopausal status of the patients and uterine atrophy. As others have reported, disruption of the junctional zone and disruption of subendometrial enhancement are the main MRI signs of myometrial infiltration, and when these signs are not clearly depicted, the diagnosis of superficial infiltration may be rather difficult and may even be impossible [2730].

Schick [18] has stated that the image quality that can be obtained with 3 T is no higher than that achieved with state-of-the-art 1.5 T. A comparison of the results of our study performed using 3-T MRI and those reported in the most recent literature using lower-field-strength MRI did not show a clear superiority of the former (Table 4), although it is possible to conclude that the overall diagnostic accuracy of 3 T is equal to the highest values obtainable at lower magnetic field intensity [14, 27, 31].


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TABLE 4: Comparison Between the Results of This Study and Those Reported in the Literature for Lower-Field-Strength MRI

 

However, the results of this study are lower than the sensitivity obtained by Nakao et al. [8] and the PPV by Cunha et al. [32]. The specificity, NPV, and diagnostic accuracy obtained at 3 T in this study are higher than those obtained with 1.5-T MRI in earlier studies, except the study performed by Cunha et al., which had 100% specificity and 93% accuracy.

The use of magnetic field strength equal to or higher than 3 T is limited in comparison with 1.5-T MRI by artifacts that may, in particular, affect abdominal and pelvic evaluations. The most commonly described artifacts are field inhomogeneity; greater magnetic susceptibility; and the dielectric effect, which is caused by reduced radiofrequency penetration power [18, 20, 22, 26].

In this study, the artifacts related to the high field significantly affected the diagnostic value of the images in nine of the 52 cases. The most significant artifacts proved to be the dielectric artifacts, which were observed in six obese patients. These artifacts, which are due to insufficient radiofrequency penetration, have been widely described [33, 34] and can be corrected by placing a gel pad on the anterior abdominal wall.

The chemical shift phenomenon is also strictly related to field strength doubles from 1.5 to 3 T [22]. In our series, chemical shift artifacts were found on the anterior and posterior surfaces of the uterus in the sagittal sequences and in the lateral bladder wall in the axial sequences, but these artifacts did not affect image quality because visualization of the zonal anatomy of the uterus was not impaired.

Magnetic susceptibility artifacts double from 1.5 to 3 T and limit the use of 3-T MRI in patients with metallic prostheses or devices [35]. In our series, these artifacts were found in four women with hip prostheses, but the artifacts did not affect diagnosis because these artifacts did not reach the uterus. Other investigators did not find a significant difference with regard to susceptibility artifacts between 1.5- and 3-T MRI of the liver [34].

The artifacts related to pelvic wall and intestinal movements can usually be reduced by positioning a rest slab on the anterior abdominal wall or by using antiperistaltic agents, respectively. In the present study, these artifacts affected the diagnostic value of the images in only three of the 52 cases. On the contrary, von Falkenhausen et al. [34] found a significant difference in the number and severity of these artifacts in evaluating the liver at 1.5 and 3 T. These artifacts are probably more common and severe in the upper abdomen than in the pelvis.

The quantity of radiofrequency deposition in human tissue was not evaluated in this study. However, sequence limitations related to specific absorption rate were not found because we used sequences with a prolonged TR and with a reduced refocusing flip angle (130°) in the T2-weighted sequences, as suggested by Morakkabati-Spitz et al. [24]. Moreover, we used parallel imaging, which reduces the quantity of radiofrequency deposition.

The results of the present study do not justify a preferential use of 3 T for the evaluation of myometrial infiltration in endometrial cancer patients, especially in light of technical, organizational, and cost issues associated with the use of this technique.

The routine use of 3-T MRI for endometrial cancer staging can be considered only if additional studies directly comparing pelvic 3- and 1.5-T MRI show a significant superiority of the former.

The results of our study suggest that 3-T MRI has a high diagnostic accuracy for endometrial cancer staging without the excessive detrimental artifacts typical of high magnetic fields. The diagnostic accuracy is equivalent to the highest accuracy values reported in the literature using 1.5-T MRI.

To prove the superiority of 3 T for endometrial cancer staging, conducting both examinations on the same cohort of patients would be necessary, with statistical validation in a larger patient population.


References
Top
Abstract
Introduction
subjects and Methods
Results
Discussion
References
 

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