Magnetic Resonance Imaging 33 (2015) 413–419
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Ultra-high-resolution MR imaging of esophageal carcinoma at ultra-high field strength (7.0 T) ex vivo: correlation with histopathologic findings☆ Ichiro Yamada a,⁎, Naoyuki Miyasaka b, Keigo Hikishima c, d, Yutaka Tokairin e, Tatsuyuki Kawano e, Eisaku Ito f, Daisuke Kobayashi f, Yoshinobu Eishi f, Hideyuki Okano c a
Department of Diagnostic Radiology and Oncology, Graduate School, Tokyo Medical and Dental University, Tokyo, Japan Department of Pediatrics, Perinatal and Maternal Medicine, Tokyo Medical and Dental University, Tokyo, Japan c Department of Physiology, Keio University School of Medicine, Tokyo, Japan d Central Institute for Experimental Animals, Kanagawa, Japan e Department of Esophagogastric Surgery, Tokyo Medical and Dental University, Tokyo, Japan f Department of Pathology, Tokyo Medical and Dental University, Tokyo, Japan b
a r t i c l e
i n f o
Article history: Received 15 May 2014 Revised 16 October 2014 Accepted 24 November 2014 Keywords: Esophagus Esophageal carcinoma Ultra-high spatial resolution Ultra-high field strength MR imaging
a b s t r a c t Purpose: To determine the usefulness of ultra-high-resolution magnetic resonance (MR) imaging at an ultra-high field strength (7.0 T), using a voxel volume of 9.5–14 nL, as means of evaluating the depth of mural invasion by esophageal carcinomas. Materials and Methods: Twenty esophageal specimens containing 20 carcinomas were studied using a 7.0-T MR imaging system with a four-channel surface coil. Ultra-high-resolution MR images were obtained with a field of view of 50–60 mm × 25–30 mm, a matrix of 512 × 256, and a section thickness of 1.0 mm, resulting in a voxel volume of 0.0095–0.014 mm3 (9.5–14 nL). Differences between tumor tissue and the esophageal wall layers and between tumor tissue and fibrosis were evaluated using visual signal intensity scoring measurements. MR images were then compared with histopathologic findings as the reference standard. Results: Ultra-high-resolution T2-weighted MR images at 7.0 T clearly depicted the normal esophageal wall in all 20 specimens (100%) as consisting of eight layers, which clearly corresponded to the tissue layers of the esophageal wall. Ultra-high-resolution T2-weighted MR images made it possible to differentiate between the tumor tissue and fibrosis clearly (P b 0.01). In all 20 esophageal carcinomas (100%), ultra-high-resolution T2-weighted MR images made it possible to determine the depth of tumor invasion in the esophageal wall as observed in the histopathologic sections. Regional lymph node involvement was also clearly depicted in four specimens. Conclusion: Ultra-high-resolution 7.0-T MR imaging, using a voxel volume of 9.5–14 nL, provides clear delineation of the esophageal wall layers, clear differentiation of tumor tissue from fibrosis, and excellent diagnostic accuracy for evaluating mural invasion by esophageal carcinomas. © 2015 Elsevier Inc. All rights reserved.
1. Introduction The prognosis of patients with esophageal carcinoma is strictly dependent on the histopathologic stage of the carcinoma [1,2], and accurate preoperative staging has a definitive impact on the selection of correct therapy for esophageal carcinoma. However, while the advent of multidetector computed tomography (CT) has ☆ Conflicts of Interest and Source of Funding: For all the authors listed, no conflicts are declared. Dr. Yamada has received the Grant-in-Aid for Scientific Research (C) of MEXT, Japan (23591753). ⁎ Corresponding author at: Department of Diagnostic Radiology and Oncology, Graduate School, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan. Tel.: +81 3 5803 5310; fax: +81 3 5803 0147. E-mail address:
[email protected] (I. Yamada). http://dx.doi.org/10.1016/j.mri.2014.11.005 0730-725X/© 2015 Elsevier Inc. All rights reserved.
contributed to the recently reported improvement in the accuracy for local staging [3,4], CT does not allow evaluation of the depth of tumor invasion in the esophageal wall, because the poor soft-tissue contrast makes it impossible to resolve the layers of the esophageal wall even with this new technology. Endoscopic ultrasound (EUS) also entails many technical limitations, including a high failure rate in stenotic tumors, high operator dependency with a recognized learning curve, artifactual interface echoes in the esophageal wall, and a limited sonographic range [5–7]. Magnetic resonance (MR) imaging is reportedly capable of visualizing mural invasion by esophageal carcinoma, and it is recognized as an alternative to CT and EUS [8–10]. However, conventional MR imaging at 1.5 T is still incapable of resolving the individual layers of the esophageal wall because of limitations in
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spatial resolution [11–16]. Ultra-high-field 7.0-T MR imaging has recently been introduced for the acquisition of ultra-high-resolution MR images in the brain and in patients with intracranial diseases [17,18]. To our knowledge, however, the use of ultra-high-resolution 7.0-T MR imaging for evaluating the depth of mural invasion by esophageal carcinomas has not been previously reported. The purpose of this study was to examine surgical specimens of the esophagus that contained an esophageal carcinoma by ultrahigh-resolution 7.0-T MR imaging, using a voxel volume of 9.5– 14 nL, to determine the signal intensity (SI) characteristics of the layers of the esophageal wall, and to assess the diagnostic accuracy of ultra-high-resolution 7.0-T MR imaging for evaluating the depth of mural invasion by esophageal carcinomas. 2. Materials and methods
ologic examination. When the observers could not fully agree on the findings, a consensus was achieved by discussion. Ultra-high-resolution MR images were reviewed for the presence, SI, uniformity, and thickness of each layer of the esophageal wall. In addition, the contour and SI of the tumor and lymph nodes were also analyzed. The degree of tumor penetration into the esophageal wall was categorized according to the layer that was invaded: mucosa, submucosa, muscularis propria, or adventitia [8]. The ultra-high-resolution MR imaging findings in the 20 esophageal specimens were compared with the histopathologic findings, which served as the reference standard. The MR images were compared with specific histopathologic sections on a sliceby-slice level, and correlations were made by visual inspection. The sensitivity, specificity, and accuracy of ultra-high-resolution MR imaging for assessing tumor invasion into each layer of the esophageal wall were then determined.
2.1. Study population 2.4. Visual SI scoring This study was approved by our institutional review board, and written informed consent was obtained from each patient. We studied 20 surgical specimens of the esophagus, each of which contained a tumor that had been histopathologically diagnosed as squamous cell carcinoma. The specimens were obtained from 20 consecutive esophageal carcinoma patients who were surgically treated at our institution. Eighteen of the 20 patients were male, and two were female. The patient ages at the time of surgery ranged from 46 years to 83 years (mean age: 66 years ± 7 [standard deviation]). The specimens in these 20 patients were analyzed and reported using the completely different techniques (diffusion-tensor MR imaging and tractography) in our previous works [19,20]. All 20 specimens were imaged after fixation in 10% formalin. Before imaging, however, the fixative was washed out of the specimens by rinsing fixed tissue with water, because the presence of formalin may alter the T2 of tissue. We did not examine the esophagus in vivo in this series. 2.2. Imaging technique Ultra-high-resolution MR imaging was performed using a 7.0-T MR imaging unit (BioSpec 70/16; Bruker BioSpin, Ettlingen, Germany) equipped with actively shielded gradients that had a maximum strength of 700 mT/m. A four-channel phased-array surface coil was used to make all the measurements. The orientation of ultra-high-resolution MR imaging was set longitudinally along the long axis of the resected segment of the esophagus. Ultra-high-resolution T2-weighted MR images were acquired using a fast spin-echo sequence with the following parameters: repetition time (TR), 3000 ms; effective echo time (TEeff), 80 ms; rapid acquisition with relaxation enhancement (RARE) factor, 4; and number of excitations (NEX), 32. Ultra-high-resolution T1-weighted MR images were also acquired using a fast spin-echo sequence with the following parameters: TR, 600 ms; TEeff, 14 ms; RARE factor, 2; and NEX, 16. All of these images were obtained with a field of view (FOV) of 50–60 mm × 25–30 mm, a matrix of 512 × 256, and a section thickness of 1.0 mm, which resulted in a voxel volume of 0.098–0.12 mm × 0.098–0.12 mm × 1.0 mm = 0.0095– 0.014 mm 3 (9.5–14 nL). The intersection gap was 1.0 mm. The acquisition times for T2-weighted and T1-weighted images were 102 minutes and 20 minutes, respectively. 2.3. Image analysis An independent, blinded evaluation of ultra-high-resolution MR images in each surgical specimen was performed by two observers (I.Y., N.M.) who had no knowledge of the results of the histopath-
Visual SI scoring was performed by comparing the SI of the layers of the esophageal wall with that of the tumor and by comparing the SI of fibrosis adjacent to the tumor and the SI of fat tissue with that of the tumor. The SI scores were classified using the following five-point scale: −2, having a markedly lower SI than that of the tumor; − 1, having a slightly lower SI than that of the tumor; 0, having an SI equal to that of the tumor; 1, having a slightly higher SI than that of the tumor; and 2, having a markedly higher SI than that of the tumor. The SI scores were averaged for each MR imaging sequence over all sections and all specimens. The results were presented as the mean ± standard deviation. We used the visual SI scoring system rather than simply computing a ratio of the SIs, because the surface coil had the different degrees of sensitivity depending on the distance from it. 2.5. Histologic preparations and examination After MR imaging, each surgical specimen was sectioned longitudinally so that the orientation of the sections corresponded to the orientation of the MR images. The sectioned specimens were embedded in paraffin and cut into 6-μm-thick slices with a microtome. These slices were then stained with hematoxylin–eosin (H-E) stain and elastica-van Gieson (EVG) stain. An experienced pathologist (E.I.) who did not have any knowledge of the MR imaging findings identified tumor invasion into each layer of the esophageal wall. 2.6. Statistical analysis All statistical analyses were performed with a commercial software package (IBM SPSS Statistics, version 20; IBM SPSS Japan, Tokyo, Japan). The one-sample Wilcoxon signed-rank test was used to determine whether the mean value of visual SI scores for the esophageal wall layers, fibrosis, and fat tissue was significantly different from zero (the zero means an equal SI for the tested tissue and the tumor tissue). The matched-pairs Wilcoxon signed-rank test was also used to evaluate significant differences between the two MR imaging sequences with respect to the visual SI scores. A P value less than 0.05 was considered to indicate a statistically significant difference. 3. Results 3.1. SI of the layers of the normal esophageal wall on ultra-highresolution MR images The SI of the layers of the normal esophageal wall on ultra-high-resolution MR images is shown in Table 1 and Fig. 1.
I. Yamada et al. / Magnetic Resonance Imaging 33 (2015) 413–419 Table 1 SI of the layers of the normal esophageal wall on ultra-high-resolution 7.0-T MR images. Tissue layer
Mucosa Epithelium Lamina propria mucosae Muscularis mucosae Submucosa Muscularis propria Inner circular muscle Intermuscular connective tissue Outer longitudinal muscle Adventitia
Ultra-high-resolution T2-weighted MR images
Ultra-high-resolution T1-weighted MR images
Low High Low High
Intermediate Intermediate Intermediate Intermediate
Low High
Intermediate Intermediate
Low High
Intermediate Intermediate
The ultra-high-resolution T2-weighted MR images of all 20 specimens (100%) clearly depicted the normal esophageal wall as consisting of the following eight layers: epithelium (low SI), lamina propria mucosae (high SI), muscularis mucosae (low SI), submucosa (high SI), inner circular muscle (low SI), intermuscular connective tissue (high SI), outer
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longitudinal muscle (low SI), and adventitia (high SI). These eight layers were found to correspond clearly to the tissue layers of the esophageal wall observed in the histologic sections. However, on the ultra-high-resolution T1-weighted MR images, all the layers of the esophageal wall had almost similar intermediate SI values in all 20 specimens, although adventitial fat tissue had a markedly high SI. 3.2. Visual SI scores on ultra-high-resolution MR images On the ultra-high-resolution T2-weighted images (Table 2), the SI of the epithelium was slightly higher than that of the tumor, with a mean SI score of 0.5 ± 0.5 (P b 0.05). The SI of the lamina propria mucosae was significantly higher than that of the tumor, with a mean SI score of 1.7 ± 0.5 (P b 0.01). The SI of the muscularis mucosae was slightly higher than that of the tumor, with a mean SI score of 0.3 ± 0.7 (not significant (N.S.)). The SI of the submucosa was significantly higher than that of the tumor, with a mean SI score of 1.9 ± 0.3 (P b 0.01). The SI of the inner circular muscle was slightly higher than that of the tumor, with a mean SI score of 0.5 ± 0.7 (N.S.). The SI of the intermuscular connective tissue was significantly higher than that of the tumor, with a mean SI score of 1.8 ± 0.4 (P b 0.01). The SI of the outer longitudinal muscle was
Fig. 1. Images of the normal esophageal wall. (a) Ultra-high-resolution T2-weighted MR image (3000/80) at 7.0 T clearly depicts the normal esophageal wall as consisting of the following eight layers: epithelium (Epi; low SI), lamina propria mucosae (LPM; high SI), muscularis mucosae (MM; low SI), submucosa (SM; high SI), inner circular muscle (ICM; low SI), intermuscular connective tissue (IMCT; high SI), outer longitudinal muscle (OLM; low SI), and adventitia (Adv; high SI). (b) Histologic section of the normal esophageal wall shows the epithelium, lamina propria mucosae, muscularis mucosae, submucosa, inner circular muscle, intermuscular connective tissue, outer longitudinal muscle, and adventitia. (Hematoxylin–Eosin stain; original magnification, ×20.)
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Table 2 SI scores of the layers of the esophageal wall compared with the esophageal carcinomas on ultra-high-resolution 7.0-T MR images. Ultra-high-resolution T2-weighted MR images
Ultra-high-resolution T1-weighted MR images
Tissue
SI score
P value
SI score
Epithelium LPM MM Submucosa ICM IMCT OLM Adventitia Fibrosis Fat tissue
0.5 1.7 0.3 1.9 0.5 1.8 0.6 1.6 −2.0 2.0
b0.05 b0.01 NS b0.01 NS b0.01 NS b0.01 b0.01 b0.01
0.0 0.1 0.0 0.3 0.1 0.4 0.1 0.9 −1.0 2.0
± ± ± ± ± ± ± ± ± ±
0.5 0.5 0.7 0.3 0.7 0.4 0.8 0.5 0.0 0.0
± ± ± ± ± ± ± ± ± ±
P value 0.0 0.3 0.0 0.5 0.3 0.5 0.3 0.6 0.0 0.0
NS NS NS NS NS b0.05 NS b0.01 b0.01 b0.01
Note. Data are the mean ± standard deviation. P values were calculated by using the one-sample Wilcoxon signed-rank test to evaluate whether the mean SI scores were significantly different from zero (a zero would mean that the SI of the tissue was equal to that of the tumor). LPM = lamina propria mucosae, MM = muscularis mucosae, ICM = inner circular muscle, IMCT = intermuscular connective tissue, OLM = outer longitudinal muscle. NS = not significant.
slightly higher than that of the tumor, with a mean SI score of 0.6 ± 0.8 (N.S.). The SI of the adventitia was significantly higher than that of the tumor, with a mean SI score of 1.6 ± 0.5 (P b 0.01).
The SI of fibrotic tissue was markedly lower than that of the tumor on ultra-high-resolution T2-weighted images, with a mean SI score of −2.0 ± 0.0 (P b 0.01). Furthermore, the SI score of the fibrotic tissue on T2-weighgted images was significantly lower than the SI scores of all the layers of the esophageal wall (P b 0.01 for all). The relative difference in SI values between fibrosis and tumor tissue on T1-weighted images was smaller (−1.0 ± 0.0; P b 0.01). When comparing the two sequences with respect to fibrosis, the SI score for T2-weighted MR images was significantly lower than that for T1-weighted MR images (P b 0.01). 3.3. Evaluation of esophageal carcinoma invasion on ultra-highresolution MR images Histopathologic examination showed that the 20 esophageal carcinomas in our series included two carcinomas confined within the mucosa (T1a), six carcinomas with invasion into the submucosa (T1b), three carcinomas with infiltration into the muscularis propria (T2), and nine carcinomas that extended into the adventitia (T3/T4). The SI of the esophageal carcinomas varied depending on the histologic components of the tumor (Figs. 2–4). The epithelial component of the tumor had low to intermediate SI values on the ultra-high-resolution T2-weighted MR images. However, associated fibrotic changes appeared as areas with markedly low SI values on the ultra-high-resolution T2-weighted images (Fig. 4). The depth of
Fig. 2. Esophageal carcinoma that has invaded the submucosa. (a) Ultra-high-resolution T2-weighted MR image (3000/80) at 7.0 T shows that an irregular low-SI tumor contrasts with the high-SI submucosal layer, and that the muscularis mucosae layer of low SI (arrows) is disrupted by the tumor. (b) Corresponding histopathologic section shows carcinoma invading the submucosal layer, which has disrupted the muscularis mucosae layer (arrows). (Hematoxylin–Eosin stain; original magnification, ×10.)
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Fig. 3. Esophageal carcinoma that has extended into the adventitia. (a) Ultra-high-resolution T2-weighted MR image (3000/80) at 7.0 T shows that a large, irregular-shaped tumor has completely disrupted the muscularis propria layer and extended into the adventitial layer (arrows). (b) Corresponding histopathologic section shows carcinoma extending into the adventitial layer (arrows). (Hematoxylin–Eosin stain; original magnification, ×4.)
invasion of the esophageal wall by all 20 carcinomas (100%) was clearly demonstrated by the ultra-high-resolution T2-weighted MR images, so they were found to be useful in assessing mural invasion by esophageal carcinomas (Table 3). On the ultra-high-resolution T2-weighted MR images, carcinomas confined within the mucosa appeared as discrete thickenings in the mucosal layer with low SI. Carcinomas invading the submucosa were demonstrated as irregular low-SI mass lesions, contrasting with the high-SI submucosa, and the low-SI muscularis mucosae layer was disrupted by the tumor lesions (Fig. 2). Carcinomas involving the muscularis propria were demonstrated to be tumors that partially replaced the muscle layer. Finally, carcinomas extending into the adventitia were demonstrated to be tumors that completely disrupted the muscularis propria layer and invaded the high-SI adventitia (Fig. 3). Ultra-high-resolution MR images also demonstrated regional lymph nodes in four specimens, and these lymph nodes were confirmed to be metastatic at histopathologic examination. The lymph nodes were clearly depicted as areas with a low SI in the adventitial fat tissue with a high SI on both ultra-high-resolution T2-weighted and T1-weighted images. 3.4. Diagnostic accuracy of ultra-high-resolution MR images Table 4 shows the performance of ultra-high-resolution MR images with respect to the assessment of invasion of the different
esophageal layers. In terms of mucosal invasion, MR images correctly diagnosed all 20 esophageal carcinomas that were studied. MR images correctly diagnosed all 18 lesions with submucosal invasion. MR images correctly diagnosed all 12 lesions with muscularis propria invasion. Finally, MR images correctly diagnosed all 9 lesions with adventitia invasion. 4. Discussion At present, ultra-high-field MR imaging at 7.0 T provides the highest field strength that is available in clinical MR imaging systems [17,18]. Since the signal-to-noise ratio (SNR) increases approximately linearly with the field strength, 7.0-T MR imaging systems have the flexibility of utilizing a higher intrinsic SNR than lower field-strength systems. The increased SNR can be traded either for better lesion contrast or for increasing the spatial resolution to identify smaller lesions [18]. Thus, ultra-high-resolution MR imaging at 7.0 T may make it possible to detect smaller lesions at earlier stages by depicting subtle pathologic changes. With its very high resolution and good contrast between different tissues, 7.0-T MR imaging has been reported to be highly accurate in detecting intracranial diseases [18]. In the present study, we performed the ultra-high-resolution MR imaging at 7.0 T, which has a voxel volume of 9.5–14 nL [17,18]. Our ultra-high-resolution MR images were found to demonstrate the detailed structures of the esophageal wall
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Fig. 4. Esophageal carcinoma that has invaded the submucosa and associated fibrotic changes in the submucosal layer adjacent to the tumor. (a) Ultra-high-resolution T2-weighted MR image (3000/80) at 7.0 T shows an irregular low-SI tumor that has invaded the submucosal layer, and areas of markedly low SI (arrows) in the submucosal layer adjacent to the tumor. (b) Corresponding histopathologic section shows carcinoma that has invaded the submucosal layer, and markedly fibrotic changes (arrows) in the submucosal layer adjacent to the tumor. (Elastica-van Gieson stain; original magnification, ×10.)
Table 3 Comparison of ultra-high-resolution 7.0-T MR images and histopathologic findings for evaluating the depth of mural invasion by esophageal carcinomas. Ultra-high-resolution MR images
Mucosa (T1a) Submucosa (T1b) Muscularis propria (T2) Adventitia (T3/T4)
Histopathologic findings Mucosa (n = 2)
Submucosa (n = 6)
Muscularis Propria (n = 3)
Adventitia (n = 9)
2 0 0 0
0 6 0 0
0 0 3 0
0 0 0 9
Note. Data are the number of lesions among 20 carcinomas in 20 patients. T1a, T1b, T2, T3, and T4 = the T component of the TNM classification for esophageal carcinoma.
Table 4 Diagnostic accuracy of ultra-high-resolution 7.0-T MR images for evaluating the depth of mural invasion by esophageal carcinomas. Depth of invasion
Sensitivity
Specificity
Accuracy
Mucosa (T1a) Submucosa (T1b) Muscularis propria (T2) Adventitia (T3/T4)
20/20 (100) 18/18 (100) 12/12 (100) 9/9 (100)
0/0 2/2 8/8 11/11
20/20 20/20 20/20 20/20
(NA) (100) (100) (100)
(100) (100) (100) (100)
Note. Data are the number of lesions. Values in parentheses are percentages. NA = not applicable.
and esophageal carcinoma because less partial volume averaging is occurring. Based on the ultra-high resolution and good tissue contrast, our data demonstrated that ultra-high-resolution MR imaging at 7.0 T makes it possible to depict the individual tissue layers of the esophageal wall clearly, to differentiate between tumor tissue and fibrosis clearly, and to determine the depth of tumor invasion in the esophageal wall. In the present study, ultra-high-resolution T2-weighted MR images at 7.0 T in all 20 specimens (100%) clearly depicted the normal esophageal wall as consisting of eight layers, and the eight layers matched the eight tissue layers of the esophageal wall observed histologically, thereby clearly demonstrating that ultra-high-resolution T2-weighted MR images at 7.0 T are capable of depicting the individual tissue layers of the esophageal wall more accurately than other imaging modalities that are available now [3–7]. In previous reports, Yamada et al. [8,9] showed that T2-weighted spin-echo MR images acquired at 1.5 T and 4.7 T also depicted six to eight layers of the esophageal wall. It is well known that the cellularity (cell density) of the adjacent layers of the normal esophageal wall differs considerably [19–22]. Therefore, the clear depiction of the layers of the normal esophageal wall on ultra-high-resolution T2-weighted images may be explained by the alternating cellularity levels of the layers, which cause significant differences in the T2 relaxation times of the layers [23].
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Our data also demonstrated that ultra-high-resolution T2-weighted MR images at 7.0 T clearly depicted fibrotic tissue as having a significantly lower SI than that of the tumor and all the layers of the esophageal wall. Thus, ultra-high-resolution T2-weighted MR images at 7.0 T were found to enable the differentiation of fibrosis from tumor tissue and the layers of the esophageal wall. Previous reports have shown that EUS tends to result in overstaging, mainly because of desmoplastic reactions or fibrosis [24,25]. Furthermore, neoadjuvant chemotherapy induces fibrosis in the esophageal wall, which is also known to cause EUS stating errors in esophageal carcinoma patients [26,27]. Therefore, the ability of ultra-high-resolution T2-weighted MR images obtained at 7.0 T to differentiate fibrosis from the tumor tissue and the layers of the esophageal wall clearly may enable a more accurate estimation of the depth of mural invasion by esophageal carcinomas, as compared with EUS. Our data demonstrated that in all 20 esophageal carcinomas (100%), ultra-high-resolution T2-weighted MR images at 7.0 T were able to diagnose the depth of invasion into the esophageal wall correctly. No overestimations or underestimations occurred in this series, although such results are frequently seen in CT and EUS [3–7]. Thus, ultrahigh-resolution T2-weighted MR images at 7.0 T were found to have a high degree of diagnostic accuracy for evaluating the depth of invasion of esophageal carcinoma. Yamada et al. [8,9] showed that T2-weighted spin-echo MR imaging in vitro could evaluate the depth of mural invasion accurately in 66 (94%) of 70 esophageal carcinomas at 4.7 T and in 39 (95%) of 41 esophageal carcinomas at 1.5 T. Conventional MR imaging has recently been used for the preoperative staging of esophageal carcinoma. Riddell et al. [13–16] performed high-spatial-resolution MR imaging with an external surface coil in esophageal carcinoma patients. Dave et al. [12] performed endoluminal MR imaging with a surface coil incorporated into the tip of an endoscope in esophageal carcinoma patients. Therefore, we think that using an external surface coil technique or endoluminal surface coil technique would make it possible to perform ultra-high-resolution MR imaging at 7.0 T in esophageal carcinoma patients. The first limitation of our study was that the specimens were imaged after fixation in formalin. In this regard, Imai et al. [28] reported that on T2-weighted MR images of the colorectal wall, the SI of the muscularis propria was slightly higher in fresh tissue than in fixed specimens and that the contrast between the submucosa and the muscularis propria was slightly reduced in fresh specimen. Auh et al. [29] reported that there was no statistical correlation between the SI and the duration of fixation in MR images of the gastric wall. Thus, we think that the data we obtained in the present study are applicable to ultra-high-resolution T2-weighted MR imaging of tissues in vivo as well as formalin-fixed tissues. The second limitation was that the imaging time in this study was considerably long, so shortening the scan time would be necessary to translate our data into in vivo ultra-high-resolution T2-weighted MR imaging. For this purpose, modifications of the pulse sequences, the development of faster MR imaging techniques, or the application of higher field strengths to clinical settings may be required in the future. As a result, ultra-high-resolution T2-weighted MR imaging at 7.0 T may provide an excellent imaging modality for the local staging of esophageal carcinoma. In conclusion, the results of the present study have demonstrated that ultra-high-resolution T2-weighted MR imaging at 7.0 T, using a voxel volume of 9.5–14 nL, provides clear delineation of the esophageal wall layers, clear differentiation of tumor tissue from fibrosis, and excellent diagnostic accuracy for assessing mural invasion by esophageal carcinomas. Thus, ultra-high-resolution T2-weighted MR imaging at 7.0 T may make it possible to diagnose the depth of mural invasion by esophageal carcinomas noninvasively.
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