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(Radiology. 2001;220:115-121.)
© RSNA, 2001

Experimental Studies

Early Gastric Carcinoma: Evaluation with High-Spatial-Resolution MR Imaging in Vitro1

Ichiro Yamada, MD, Naoya Saito, MD, Kimiya Takeshita, MD, Norio Yoshino, DDS, Akemi Tetsumura, DDS, Jiro Kumagai, MD and Hitoshi Shibuya, MD

1 From the Departments of Radiology (I.Y., H.S.), Surgery (N.S., K.T.), and Pathology (J.K.), Faculty of Medicine, and the Department of Dental Radiology Faculty of Dentistry, (N.Y., A.T.), Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan. Received August 19, 2000; revision requested September 26; revision received November 16; accepted January 8, 2001. Address correspondence to I.Y. (e-mail: yamada.crad@med.tmd.ac.jp).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
PURPOSE: To determine signal intensity characteristics of the gastric wall layers and to assess the accuracy of the evaluation of early gastric carcinomas in vitro by using resected specimens studied with high-spatial-resolution magnetic resonance (MR) imaging.

MATERIALS AND METHODS: Fifteen gastric specimens obtained from patients suspected of having early gastric carcinoma were studied with a 1.5-T MR system with a 4-cm-diameter loop coil. High-spatial-resolution spin-echo MR images were obtained with a field of view of 50 mm, a matrix of 256 x 256, and a section thickness of 2 mm, resulting in a voxel size of 0.08 mm3. Findings from MR images were compared with histopathologic findings.

RESULTS: T1- and T2-weighted MR images clearly depicted the normal gastric wall as consisting of four and six layers, respectively, which corresponded well to the histologic layers. In 14 (93%) of 15 gastric carcinomas, the depth of mural invasion visualized with MR imaging correlated well with the histopathologic stage. The stage determined with MR imaging, however, was lower in one instance (7%) than the histopathologic stage. MR imaging also depicted the gross features of the tumor, presence of ulceration, and adjacent lymph node swelling.

CONCLUSION: High-spatial-resolution MR imaging has a high diagnostic accuracy in the evaluation of the mural invasion of early gastric carcinoma in vitro and thus potentially enables preoperative histopathologic staging.

Index terms: Magnetic resonance (MR), tissue characterization, 72.121411, 72.32 • Specimens, MR, 72.32 • Stomach, MR, 72.121411 • Stomach, neoplasms, 72.32


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
The rate of early gastric carcinoma (T1 stage) (1) relative to the incidence of all gastric carcinomas has increased in Japan (2). The prognosis for patients with early gastric carcinoma is strictly dependent on the depth of carcinoma invasion in the gastric wall (2,3). Accurate preoperative staging has a definite influence on the selection of the correct therapy for early gastric carcinoma. Staging of gastric cancer has been performed by using computed tomography (CT) or ultrasonography (US) (4). However, to accurately assess the depth of carcinoma invasion in the gastric wall, the layers of the gastric wall must be distinctly depicted. Endoscopic US has been used to examine the gastric wall, but its diagnostic accuracy for tumor staging is still controversial (4–6). Thus, diagnostic imaging for evaluating early gastric carcinoma is limited, at present.

Recently, high-spatial-resolution magnetic resonance (MR) imaging has been widely used in vitro as a research tool for assessing the signal intensity characteristics of an excised organ or tumor (7–11). However, to our knowledge, high-spatial-resolution MR imaging has not been used specifically to study presumed early gastric carcinoma. The purpose of this study was to determine the signal intensity characteristics of the gastric wall layers and to assess the accuracy of the evaluation of early gastric carcinomas in vitro by using resected specimens that were studied with high-spatial-resolution MR imaging.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Study Group
We studied 15 resected gastric specimens containing 15 tumor lesions that were histopathologically confirmed to be adenocarcinoma. The gastric specimens studied were obtained from 15 consecutive patients suspected of having early gastric carcinoma who underwent surgery at our institution. No other histologic types were found in this series. Ten of these patients were men and five were women. Their age at the time of surgery ranged from 46 to 77 years (mean age, 64 years ± 8 [SD]). The specimens were entire gastric resections in six patients and partial gastric resections in nine patients. In all the specimens, just the part with carcinoma was imaged in this study. The study protocol was approved by the institutional review board, and informed consent was obtained from all patients for the study of their resected specimens. All specimens were imaged after fixation in formalin. We did not examine the specimens in vivo in this series.

Imaging Technique
High-spatial-resolution MR imaging was performed by using a 1.5-T superconducting system with a 25 mT/m maximum gradient capability (Magnetom Vision; Siemens, Erlangen, Germany) and a 4-cm-diameter loop coil. Conventional single-section sagittal, coronal, and transverse scout images of the gastric specimens were initially obtained.

In all specimens, T1-weighted spin-echo MR images were obtained with a 500/20 (repetition time msec/echo time msec) sequence and with eight signals acquired. T2-weighted spin-echo MR images were obtained with a 2,000/70 sequence and with four signals acquired. All of these images were obtained with a field of view of 50 x 50 mm, a matrix of 256 x 256, and a section thickness of 2 mm, which resulted in a voxel size of 0.2 x 0.2 x 2.0 mm equaling 0.08 mm3. The intersection gap was 0.5 mm. Acquisition times for T1- and T2-weighted images were 17 minutes 4 seconds and 34 minutes 8 seconds, respectively. The orientation of both the T1- and T2-weighted images was along the longitudinal axis of the resected stomach so that the entire tumor lesion was imaged.

Image Analysis
The diagnostic accuracy in vitro was evaluated with separate interpretations of the MR images made by two independent observers (I.Y., N.Y.). The MR images were independently interpreted without knowledge of the histopathologic findings. When the observers did not fully agree with the findings, the diagnosis was made with discussion. To assess interobserver variability in image interpretation, the {kappa} statistic was used to measure the degree of agreement between the two observers. In addition, none of the specimens were normal, and the MR reviewers were not blinded to this fact; this might be a source of bias. The observers were not blinded to the suspicion of gastric carcinoma, and they had knowledge of where in the specimen carcinoma was suspected, because the specific part with carcinoma was imaged.

MR imaging findings were reviewed for the signal intensity, uniformity, and thickness of each layer of the gastric wall. In addition, the contour and the signal intensity of the tumors and lymph nodes were also analyzed. The degree of tumor penetration into the gastric wall was categorized according to the layer invaded: mucosa, submucosa, muscularis propria, or subserosa or serosa.

The MR imaging criteria used by the observers to determine the depth of involvement were as follows: (a) discrete mass(es) present in the layers, (b) focal areas of abnormal signal intensity within the thickened layers, and (c) mucosal ulcerations with surrounding or underlying mass(es) (8).

The findings from high-spatial-resolution MR imaging of the 15 tumors were compared with the histopathologic findings, which served as the standard. The two observers together (I.Y., N.Y.) compared MR images with specific histopathologic sections, and correlations were made with visual analysis. The sensitivity, specificity, and accuracy of high-spatial-resolution MR imaging for assessing tumor invasion into each layer of the gastric wall were then determined. Furthermore, the MR imaging and histologic stages were compared by using the Spearman correlation coefficient in the two groups. P values of less than .05 were considered to indicate a statistically significant difference.

Histologic Preparations and Examination
After MR imaging, the specimen of the resected stomach was sectioned longitudinally along the long axis of the stomach to correspond to the orientation of the MR images. The specimen was then embedded in paraffin and cut into 6-µm-thick sections with a microtome. These sections were then stained with hematoxylin-eosin. Carcinoma invasion into each layer of the gastric wall was diagnosed by an experienced pathologist (J.K.) who was unaware of the findings of the MR imaging.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Signal Intensity Characteristics of the Normal Gastric Wall
The signal intensity of the layers of the normal gastric wall is summarized in Table 1. On T1-weighted high-spatial-resolution MR images, the mucosa and submucosa in the gastric wall had a low signal intensity, but fat tissue in the submucosa showed a high signal intensity (Fig 1). The muscularis propria and subserosa or serosa had a low signal intensity, but fat tissue in the subserosa showed a high signal intensity.


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  		TABLE 1. Signal Intensity of the Layers of the Normal Gastric Wall at High-Spatial-Resolution MR Imaging

 


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  		Figure 1a. Images depict the four layers of the normal gastric wall: mucosa (m), submucosa (sm), muscularis propria (mp), and subserosa or serosa (s). (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20). The high signal intensity (*) in the submucosa indicates submucosal fat tissue. The low-signal-intensity lines (straight arrows) in the upper and lower submucosa indicate submucosal areas without fat tissue. The low-signal-intensity line (curved arrow) in the muscularis propria indicates the intermuscular connective tissue. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70). The muscularis propria consists of inner circular muscle, intermuscular connective tissue (curved arrow), and outer longitudinal muscle. The low signal intensity (*) in the submucosa indicates submucosal fat tissue. The high-signal-intensity lines (straight arrows) in the upper and lower submucosa indicate submucosal areas without fat tissue. (c) Photomicrograph. The muscularis propria consists of inner circular muscle, intermuscular connective tissue (arrow), and outer longitudinal muscle. (Hematoxylin-eosin stain; original magnification, x1.8.)

 


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  		Figure 1b. Images depict the four layers of the normal gastric wall: mucosa (m), submucosa (sm), muscularis propria (mp), and subserosa or serosa (s). (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20). The high signal intensity (*) in the submucosa indicates submucosal fat tissue. The low-signal-intensity lines (straight arrows) in the upper and lower submucosa indicate submucosal areas without fat tissue. The low-signal-intensity line (curved arrow) in the muscularis propria indicates the intermuscular connective tissue. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70). The muscularis propria consists of inner circular muscle, intermuscular connective tissue (curved arrow), and outer longitudinal muscle. The low signal intensity (*) in the submucosa indicates submucosal fat tissue. The high-signal-intensity lines (straight arrows) in the upper and lower submucosa indicate submucosal areas without fat tissue. (c) Photomicrograph. The muscularis propria consists of inner circular muscle, intermuscular connective tissue (arrow), and outer longitudinal muscle. (Hematoxylin-eosin stain; original magnification, x1.8.)

 


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  		Figure 1c. Images depict the four layers of the normal gastric wall: mucosa (m), submucosa (sm), muscularis propria (mp), and subserosa or serosa (s). (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20). The high signal intensity (*) in the submucosa indicates submucosal fat tissue. The low-signal-intensity lines (straight arrows) in the upper and lower submucosa indicate submucosal areas without fat tissue. The low-signal-intensity line (curved arrow) in the muscularis propria indicates the intermuscular connective tissue. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70). The muscularis propria consists of inner circular muscle, intermuscular connective tissue (curved arrow), and outer longitudinal muscle. The low signal intensity (*) in the submucosa indicates submucosal fat tissue. The high-signal-intensity lines (straight arrows) in the upper and lower submucosa indicate submucosal areas without fat tissue. (c) Photomicrograph. The muscularis propria consists of inner circular muscle, intermuscular connective tissue (arrow), and outer longitudinal muscle. (Hematoxylin-eosin stain; original magnification, x1.8.)

 
Thus, T1-weighted high-spatial-resolution MR images depicted the normal gastric wall as consisting of the four layers that corresponded well to the histologic layers of the gastric wall: mucosa (low signal intensity), submucosa (low or high signal intensity), muscularis propria (low signal intensity), and subserosa or serosa (low or high signal intensity) (Table 1).

On T2-weighted high-spatial-resolution MR images, the mucosa had a low signal intensity, the submucosa had a high signal intensity, but the fat tissue in the submucosa showed a low signal intensity (Fig 1). T2-weighted high-spatial-resolution MR images depicted the muscularis propria as three layers. The inner circular and outer longitudinal muscle layers were seen as discrete low-signal-intensity structures, which were separated by a thin, high-signal-intensity band that correlated with the loose connective tissue. The subserosa or serosa had a high signal intensity, but fat tissue in the subserosa showed a low signal intensity.

Thus, T2-weighted high-spatial-resolution MR images depicted the normal gastric wall as consisting of the six layers that corresponded well to the histologic layers of the gastric wall: mucosa (low signal intensity), submucosa (high or low signal intensity), inner circular muscle (low signal intensity), intermuscular connective tissue (high signal intensity), outer longitudinal muscle (low signal intensity), and subserosa or serosa (high or low signal intensity) (Table 1).

The pathologic specimens appeared different from the normal example in areas remote from the tumor, because submucosal fat tissue was different among the specimens. Thus, the pathologic sections in some parts seemed to have fewer layers that were depicted at MR imaging, but otherwise all 15 specimens showed the signal intensity results listed in Table 1. The combined reading of both T1- and T2-weighted images was useful in the identification of the layers of the gastric wall.

Evaluation of Gastric Carcinoma Invasion
The 15 gastric carcinomas in this series included six carcinomas confined within the mucosa, three that invaded the submucosa, two that infiltrated the muscularis propria, and four that penetrated through the muscularis propria and extended into the subserosa or serosa (Table 2). The signal intensities of the gastric carcinomas varied depending on the histologic components of the tumors (Figs 2–5). The epithelial component of the tumor had low signal intensity on the T1-weighted images and low to intermediate signal intensity on the T2-weighted images. However, associated fibrotic change appeared as areas of low signal intensity on both the T1- and T2-weighted images.


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  		TABLE 2. High-Spatial-Resolution MR Imaging and Histopathologic Findings in the Evaluation of the Depth of Gastric Carcinoma Invasion

 


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  		Figure 2a. Early gastric carcinoma of superficial elevated type confined within the mucosa. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows an elevated lesion (straight arrow) in the mucosa, and the submucosa (curved arrow) high signal intensity appears to be intact. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows an elevated lesion (straight arrow) in the mucosa, and the submucosa (curved arrow) of low signal intensity appears to be intact. (c) Photomicrograph shows carcinoma confined within the mucosa, as well as intact submucosa (arrow). (Hematoxylin-eosin stain; original magnification, x1.8.)

 


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  		Figure 2b. Early gastric carcinoma of superficial elevated type confined within the mucosa. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows an elevated lesion (straight arrow) in the mucosa, and the submucosa (curved arrow) high signal intensity appears to be intact. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows an elevated lesion (straight arrow) in the mucosa, and the submucosa (curved arrow) of low signal intensity appears to be intact. (c) Photomicrograph shows carcinoma confined within the mucosa, as well as intact submucosa (arrow). (Hematoxylin-eosin stain; original magnification, x1.8.)

 


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  		Figure 2c. Early gastric carcinoma of superficial elevated type confined within the mucosa. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows an elevated lesion (straight arrow) in the mucosa, and the submucosa (curved arrow) high signal intensity appears to be intact. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows an elevated lesion (straight arrow) in the mucosa, and the submucosa (curved arrow) of low signal intensity appears to be intact. (c) Photomicrograph shows carcinoma confined within the mucosa, as well as intact submucosa (arrow). (Hematoxylin-eosin stain; original magnification, x1.8.)

 


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  		Figure 3a. Early gastric carcinoma of superficial depressed type confined within the mucosa. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows a depressed lesion (straight arrows) in the mucosa, and the submucosa (curved arrow) of high signal intensity appears to be intact. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows a depressed lesion (straight arrows) in the mucosa, and the submucosa (curved arrow) of low signal intensity appears to be intact. (c) Photomicrograph shows carcinoma confined within the mucosa, as well as intact submucosa (arrow). (Hematoxylin-eosin stain; original magnification, x1.4.)

 


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  		Figure 3b. Early gastric carcinoma of superficial depressed type confined within the mucosa. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows a depressed lesion (straight arrows) in the mucosa, and the submucosa (curved arrow) of high signal intensity appears to be intact. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows a depressed lesion (straight arrows) in the mucosa, and the submucosa (curved arrow) of low signal intensity appears to be intact. (c) Photomicrograph shows carcinoma confined within the mucosa, as well as intact submucosa (arrow). (Hematoxylin-eosin stain; original magnification, x1.4.)

 


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  		Figure 3c. Early gastric carcinoma of superficial depressed type confined within the mucosa. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows a depressed lesion (straight arrows) in the mucosa, and the submucosa (curved arrow) of high signal intensity appears to be intact. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows a depressed lesion (straight arrows) in the mucosa, and the submucosa (curved arrow) of low signal intensity appears to be intact. (c) Photomicrograph shows carcinoma confined within the mucosa, as well as intact submucosa (arrow). (Hematoxylin-eosin stain; original magnification, x1.4.)

 


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  		Figure 4a. Early gastric carcinoma of superficial elevated type invading the submucosa. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows that an irregularly shaped, low-signal-intensity tumor (short straight arrows) contrasts with the high-signal-intensity submucosa (curved arrow), which has an irregular narrowing. There is a difference between the signal intensities from the epithelial component (short straight arrows) and the fibrotic changes (long straight arrow) associated with the tumor. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows that an irregularly shaped tumor (short straight arrows) contrasts with the submucosa (curved arrow) of lower signal intensity, which has an irregular narrowing. There is a difference between the signal intensity from the epithelial component (short straight arrows) and that from the fibrotic changes (long straight arrow) associated with the tumor. (c) Photomicrograph shows carcinoma (thick straight arrows) invading the submucosa (curved arrow). There are epithelial components (thick straight arrows) and fibrotic changes (thin straight arrow). (Hematoxylin-eosin stain; original magnification, x1.5.)

 


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  		Figure 4b. Early gastric carcinoma of superficial elevated type invading the submucosa. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows that an irregularly shaped, low-signal-intensity tumor (short straight arrows) contrasts with the high-signal-intensity submucosa (curved arrow), which has an irregular narrowing. There is a difference between the signal intensities from the epithelial component (short straight arrows) and the fibrotic changes (long straight arrow) associated with the tumor. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows that an irregularly shaped tumor (short straight arrows) contrasts with the submucosa (curved arrow) of lower signal intensity, which has an irregular narrowing. There is a difference between the signal intensity from the epithelial component (short straight arrows) and that from the fibrotic changes (long straight arrow) associated with the tumor. (c) Photomicrograph shows carcinoma (thick straight arrows) invading the submucosa (curved arrow). There are epithelial components (thick straight arrows) and fibrotic changes (thin straight arrow). (Hematoxylin-eosin stain; original magnification, x1.5.)

 


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  		Figure 4c. Early gastric carcinoma of superficial elevated type invading the submucosa. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows that an irregularly shaped, low-signal-intensity tumor (short straight arrows) contrasts with the high-signal-intensity submucosa (curved arrow), which has an irregular narrowing. There is a difference between the signal intensities from the epithelial component (short straight arrows) and the fibrotic changes (long straight arrow) associated with the tumor. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows that an irregularly shaped tumor (short straight arrows) contrasts with the submucosa (curved arrow) of lower signal intensity, which has an irregular narrowing. There is a difference between the signal intensity from the epithelial component (short straight arrows) and that from the fibrotic changes (long straight arrow) associated with the tumor. (c) Photomicrograph shows carcinoma (thick straight arrows) invading the submucosa (curved arrow). There are epithelial components (thick straight arrows) and fibrotic changes (thin straight arrow). (Hematoxylin-eosin stain; original magnification, x1.5.)

 


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  		Figure 5a. Advanced gastric carcinoma involving the muscularis propria. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows that an irregularly shaped tumor partially replaces the muscularis propria (curved arrow) but does not penetrate through the muscularis propria. In addition, a deep ulceration (straight arrow) is seen in the central part of the tumor. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows that an irregularly shaped tumor partially replaces the muscularis propria layer (curved arrow), but that it does not penetrate through the muscularis propria layer. In addition, a deep ulceration (straight arrow) is seen in the central part of the tumor. (c) Photomicrograph shows carcinoma involving the muscularis propria (curved arrow), which manifests a deep ulceration (straight arrow) in the central part. (Hematoxylin-eosin stain; original magnification, x1.5.)

 


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  		Figure 5b. Advanced gastric carcinoma involving the muscularis propria. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows that an irregularly shaped tumor partially replaces the muscularis propria (curved arrow) but does not penetrate through the muscularis propria. In addition, a deep ulceration (straight arrow) is seen in the central part of the tumor. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows that an irregularly shaped tumor partially replaces the muscularis propria layer (curved arrow), but that it does not penetrate through the muscularis propria layer. In addition, a deep ulceration (straight arrow) is seen in the central part of the tumor. (c) Photomicrograph shows carcinoma involving the muscularis propria (curved arrow), which manifests a deep ulceration (straight arrow) in the central part. (Hematoxylin-eosin stain; original magnification, x1.5.)

 


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  		Figure 5c. Advanced gastric carcinoma involving the muscularis propria. (a) Sagittal T1-weighted high-spatial-resolution spin-echo MR image (500/20) shows that an irregularly shaped tumor partially replaces the muscularis propria (curved arrow) but does not penetrate through the muscularis propria. In addition, a deep ulceration (straight arrow) is seen in the central part of the tumor. (b) Sagittal T2-weighted high-spatial-resolution spin-echo MR image (2,000/70) shows that an irregularly shaped tumor partially replaces the muscularis propria layer (curved arrow), but that it does not penetrate through the muscularis propria layer. In addition, a deep ulceration (straight arrow) is seen in the central part of the tumor. (c) Photomicrograph shows carcinoma involving the muscularis propria (curved arrow), which manifests a deep ulceration (straight arrow) in the central part. (Hematoxylin-eosin stain; original magnification, x1.5.)

 
The depth of carcinoma invasion into the gastric wall was well demonstrated with high-spatial-resolution MR imaging. Both T1- and T2-weighted MR images were useful in the assessment of tumor invasion into the wall of the stomach. On both T1- and T2-weighted MR images, carcinomas confined within the mucosa appeared as discrete thickening in the mucosal layer with low signal intensity (Figs 2, 3). However, the submucosa was intact in these mucosal tumors. Carcinomas invading the submucosa were demonstrated as irregular low-signal-intensity mass lesions contrasting with the high- and low-signal-intensity submucosa on the T1- and T2-weighted MR images, respectively (Fig 4). Carcinomas involving the muscularis propria were demonstrated to be tumor lesions that partially replaced the muscularis propria layer (Fig 5). Finally, carcinomas extending into the subserosa or serosa were demonstrated to be tumor lesions that completely disrupted the muscularis propria layer, as well as superficial layers, and also invaded the subserosa or serosa layer.

As shown in Table 2, in 14 (93%) of 15 gastric carcinomas, the results of the depth of mural invasion obtained with high-spatial-resolution MR imaging accurately correlated with the results of histopathologic staging. The stage determined with MR imaging, however, was lower in one (7%) carcinoma. MR imaging caused underestimation in one carcinoma involving the subserosa as invading the muscularis propria. In this one lesion, the cancerous involvement of the subserosa was so microscopic that this slight involvement was missed at MR imaging.

High-spatial-resolution MR imaging also demonstrated regional lymph nodes in two patients, and they were confirmed to be metastatic at histopathologic examination. The lymph nodes were clearly depicted as having low signal intensity in the subserosal fat tissue on T1-weighted high-spatial-resolution MR images. However, on T2-weighted high-spatial-resolution MR images, the lymph nodes in the subserosal fat tissue were obscured because of decreased contrast between the lymph node and the fat tissue.

Diagnostic Accuracy of High-Spatial-Resolution MR Imaging
Table 3 shows the diagnostic accuracy of high-spatial-resolution MR imaging in the evaluation of gastric carcinoma invasion. MR imaging correctly aided in the diagnosis of all 15 gastric carcinomas studied, in terms of mucosal invasion. MR imaging correctly depicted all nine lesions with submucosal invasion. MR imaging correctly depicted all six lesions with muscularis propria invasion. Finally, MR imaging correctly depicted three of four lesions with subserosal or serosal invasion, but in one other lesion, a false-negative finding was obtained. The Spearman correlation coefficient of 0.98 was obtained between the MR imaging and histologic staging (P < .001), and, thus, the correspondence was excellent.


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  		TABLE 3. Diagnostic Accuracy of High-Spatial-Resolution MR Imaging in the Evaluation of Gastric Carcinoma Invasion

 
Furthermore, high-spatial-resolution MR imaging accurately depicted nine (60%) early and six (40%) advanced gastric carcinomas (Table 4). These results demonstrated that high-spatial-resolution MR imaging helped to differentiate between early and advanced gastric carcinomas with a high degree of diagnostic accuracy.


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  		TABLE 4. Diagnostic Accuracy of High-Spatial-Resolution MR Imaging for Differentiation between Early and Advanced Gastric Carcinomas

 
In two (13%) of 15 lesions, the observers did not agree with their findings, and the diagnosis was made with discussion. {kappa} value of 0.82 was obtained between the two observers, and, thus, interobserver agreement for gastric carcinoma invasion was excellent.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
The prognosis for patients with early gastric carcinoma is strictly dependent on the depth of the carcinoma invasion in the gastric wall (2,3). Accurate preoperative staging also has a definite influence on the selection of the correct therapy for early gastric carcinoma. Thus, preoperative diagnosis of the depth of carcinoma invasion is important in the treatment of patients with early gastric carcinoma. However, preoperative staging of early gastric carcinoma has been severely limited by the fact that available imaging modalities do not enable evaluation of the true extent of invasion in the gastric wall (4–6).

Endoscopic US has been used in the evaluation of gastric carcinoma. However, depending on the US probe used, the normal gastric wall has been described (4–6) as consisting of five to nine layers. Such a discrepancy between the US and histologic findings is due to additional echoes produced by the interfaces between different histologic layers (4–6). These artifacts appear to cause a misevaluation of the depth of gastric carcinoma invasion. Another problem is that the results of endoscopic US are highly operator-dependent, and tumor invasion results obtained by different operators may differ, even in the same patient. Therefore, a more reliable, easier method for evaluating tumor invasion is needed for preoperative staging of early gastric carcinoma.

Our data have demonstrated that in vitro T1- and T2-weighted high-spatial-resolution MR images clearly depict the normal gastric wall as consisting of four and six layers, respectively, which corresponds well with the actual histologic layers of the gastric wall. MR imaging causes higher soft-tissue contrast than do other imaging modalities, and it does not cause the artifactual interface echoes in the gastric wall that are seen with endoscopic US. Thus, high-spatial-resolution MR imaging may help to differentiate the normal layers of the gastric wall more accurately than other imaging modalities (4–6). However, this conclusion is based on the comparison of results obtained with endoscopic US in actual patients, with the results of this study based on MR evaluation of fixed specimens. Surely, a more valid comparison would involve grading of the same excised tissue specimens in vitro with both MR imaging and US.

Auh et al (8) studied the gastric wall with a 4.7-T experimental system, which showed three layers of the gastric wall. Thus, our results demonstrate that high-spatial-resolution MR images obtained at 1.5 T distinctly depict the actual histologic layers of the gastric wall.

Our data have demonstrated that in 14 (93%) of the 15 gastric carcinomas studied, high-spatial-resolution MR imaging was able to correctly depict the depth of invasion in the gastric wall. MR imaging caused underestimation of one other (7%) carcinoma invading the subserosa as involving the muscularis propria. The Spearman correlation coefficient between the MR imaging and histologic staging was 0.98, and the correspondence was excellent. Furthermore, high-spatial-resolution MR imaging accurately depicted nine (60%) early and six (40%) advanced gastric carcinomas. Our results also demonstrate that high-spatial-resolution MR imaging helped to differentiate between early and advanced gastric carcinomas with a high degree of diagnostic accuracy.

The 5-year survival rate in patients with early gastric carcinoma is significantly superior to that in patients with advanced gastric carcinomas (12,13). Furthermore, the outcome of early gastric carcinoma limited to the mucosa is significantly better than that of early gastric carcinomas with submucosal invasion (14,15). Thus, differentiation between early and advanced carcinomas and between mucosal and submucosal carcinomas is markedly important in the preoperative estimation of prognosis in patients with gastric carcinoma. In this regard, our results show that high-spatial-resolution MR imaging demonstrates a high degree of diagnostic accuracy in the evaluation of the depth of invasion of early gastric carcinomas. Recently, Auh et al (8) showed that 4.7-T MR imaging in vitro could accurately aid in the evaluation of the depth of mural invasion in seven of a group of eight gastric carcinomas, which included only two early carcinomas.

Furthermore, the choice of treatment for early gastric carcinoma depends on the depth of invasion (12–15). For patients with early gastric carcinoma limited to the mucosa, local gastric resection or gastrectomy with perigastric lymph node dissection may be sufficient to cure the disease, because these patients rarely have metastasis. For small, early gastric carcinoma, endoscopic mucosal resection may also be taken into consideration (12–15). By means of high-spatial-resolution MR imaging, which has a high diagnostic accuracy for depicting the depth of carcinoma invasion, it may be possible to adopt a smaller operation or endoscopic mucosal resection for cases with early gastric carcinomas without lymph node metastasis.

The first limitation of our study was that the specimens were imaged after fixation in formalin. In this regard, Imai et al (7) reported that on T2-weighted images of the colorectal wall, the signal intensity of the muscularis propria was somewhat higher in fresh specimens than in fixed specimens and that the contrast between the submucosa and the muscularis propria was somewhat reduced on images of fresh specimens. Auh et al (8) reported that no statistical correlation existed between the signal intensity and the duration of fixation in MR imaging of the stomach wall. Ideally, a comparison between fresh and fixed specimens must be done for the stomach in an adequate number of specimens, and a correlation between the appearance in vitro and in vivo must be done. In this preliminary study, however, no consideration was given to the attempt to image these patients preoperatively as well.

The second limitation was that the observers were not blinded to the diagnosis of carcinoma only to the histologic depth of invasion. Thus, this study attempted to validate high-spatial-resolution MR imaging only as a confirmatory test, not as a screening examination.

The third limitation was that the examination times were inordinately long and would not work in the present configuration in vivo. In this regard, clinical high-spatial-resolution MR imaging in vivo already has been used (16,17) for the staging of rectal cancer. Chan et al (16) reported in their study of rectal cancer, in which they used an endorectal surface coil, that four layers of the wall were depicted on T2-weighted images and that accurate tumor staging was possible in 11 of 12 patients.

In comparison with the imaging of rectal cancer, there are more technical issues associated with using preoperative gastric imaging in vivo, including motion (peristalsis, respiratory motion, and gross patient motion), necessity for gastric distention, and limitation on lumen contents. Clinical application of high-spatial-resolution MR imaging of the stomach is still in the preliminary stage (18–21). We believe that high-spatial-resolution MR imaging of early gastric carcinomas in vivo will be possible in the near future with the development of faster MR imaging techniques and with the use of an endoluminal surface-coil technique guided with endoscopy or a body-coil technique with a reduced or targeted field of view (18–22).

In conclusion, the present study findings have demonstrated that high-spatial-resolution MR imaging in vitro clearly depicts the internal architecture of the gastric wall and has a high diagnostic accuracy in the evaluation of the mural invasion of early gastric carcinoma.

Practical application: Further research is needed when endoluminal surface coil technology is available. However, high-spatial-resolution MR imaging might enable preoperative histopathologic staging of early gastric carcinoma.


   FOOTNOTES
 
Author contributions: Guarantor of integrity of entire study, I.Y.; study concepts, I.Y., N.S.; study design, I.Y., N.Y.; literature research, I.Y.; experimental studies, I.Y., N.Y.; data acquisition and analysis/interpretation, I.Y., N.Y.; statistical analysis, I.Y., A.T.; manuscript preparation and definition of intellectual content, I.Y., J.K.; manuscript editing, I.Y., A.T.; manuscript revision/review, K.T., A.T.; manuscript final version approval, I.Y., H.S.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 

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