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Published online before print December 19, 2007, 10.1148/radiol.2462070128

(Radiology 2007;246:444.)

A more recent version of this article appeared on December 1, 2007
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© RSNA, 2007

Experimental Studies

Colorectal Carcinoma: In Vitro Evaluation with High-Spatial-Resolution 3D Constructive Interference in Steady-State MR Imaging1

Ichiro Yamada, MD, Satoshi Okabe, MD, Masayuki Enomoto, MD, Kenichi Sugihara, MD, Norio Yoshino, DDS, Akemi Tetsumura, DDS, Jiro Kumagai, MD, and Hitoshi Shibuya, MD

1 From the Departments of Diagnostic Radiology and Oncology (I.Y., H.S.), Surgery (S.O., M.E., K.S.), Oral and Maxillofacial Radiology (N.Y., A.T.), and Pathology (J.K.), Graduate School, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan. From the 2006 RSNA Annual Meeting. Received January 19, 2007; revision requested March 16; revision received March 26; accepted May 2; final version accepted July 24. Address correspondence to I.Y. (e-mail: yamada.crad{at}tmd.ac.jp).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Purpose: To retrospectively assess the accuracy of high-spatial-resolution three-dimensional (3D) constructive interference in steady-state (CISS) magnetic resonance (MR) imaging in the evaluation of mural invasion of colorectal carcinoma by using prospectively obtained in vitro images, with histopathologic analysis as the reference standard.

Materials and Methods: Institutional review board approval was obtained for the prospective and retrospective components of this study, with informed consent for the former and waiver of informed consent for the latter. Surgical specimens were obtained in 92 patients (61 men, 31 women; mean age, 65 years) and contained 96 colorectal carcinomas. Specimens were examined with a 1.5-T MR system and a 4-cm-diameter loop coil. High-spatial-resolution 3D CISS MR images were obtained with 80 x 80-mm field of view, 512 x 512 matrix, and 0.7-mm section thickness, which resulted in a 0.017-mm3 voxel size. The 3D data sets were postprocessed with surface-rendering software to generate virtual MR endoscopic images. The 3D CISS MR images were compared with histopathologic findings, and virtual MR endoscopic images were compared with macroscopic findings at surgery. Statistical analysis was performed with Spearman rank correlation.

Results: In 92 (96%) colorectal carcinomas, the depth of mural invasion depicted by 3D CISS MR imaging correlated well with the histopathologic stage, although the stage assigned with 3D CISS MR imaging was higher than that assigned with histopathologic analysis in four (4%) carcinomas (r = 0.976, P < .001). Sensitivity, specificity, and accuracy were 100%, 94%–96%, and 98%–100%, respectively. In 91 (95%) carcinomas, virtual MR endoscopy clearly depicted the macroscopic type of carcinoma, including gross configuration and tumor ulceration (r = 0.916, P < .001).

Conclusion: High-spatial-resolution 3D CISS MR imaging has high diagnostic accuracy in the in vitro evaluation of mural invasion and macroscopic features of colorectal carcinomas.

© RSNA, 2007


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Colorectal carcinoma is one of the most common malignant neoplasms worldwide, and the prognosis of patients with this disease depends strictly on the pathologic stage of cancer (1,2). Accurate preoperative staging of colorectal carcinoma has a definite effect on the selection of the most appropriate therapy. Computed tomography and ultrasonography (US) have been used for staging (3); however, the depth of tumor invasion—which is one of the most important factors in staging—cannot be reliably evaluated with these methods. To accurately assess the depth of carcinoma in the colorectal wall, the layers of the colorectal wall must be depicted clearly. Endoscopic US has been used to examine the colorectal wall, but the accuracy of tumor staging with endoscopic US is still controversial (3–7). Thus, the diagnostic methods currently available to evaluate depth of invasion are limited.

Previous reports have described the usefulness and limitations of T2-weighted magnetic resonance (MR) imaging in the evaluation of mural invasion of colorectal carcinoma (8–10); however, the spatial resolution of conventional spin-echo MR imaging for depicting detailed structures is limited. Three-dimensional (3D) constructive interference in steady-state (CISS) MR imaging has been used to obtain high-spatial-resolution and heavily T2-weighted images in patients with intracranial diseases and esophageal carcinoma (11–13). To our knowledge, however, there have been no reports on the use of 3D CISS MR imaging to evaluate colorectal carcinoma. Thus, the purpose of our study was to retrospectively assess the accuracy of high-spatial-resolution 3D CISS MR imaging in the evaluation of mural invasion of colorectal carcinoma by using prospectively obtained in vitro images, with histopathologic analysis as the reference standard.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
We obtained institutional review board approval for the prospective and retrospective components of our study, with informed consent for the former and waiver of informed consent for the latter. We used 92 surgical specimens that contained 96 colorectal tumors. These specimens had been prospectively obtained in 92 consecutive patients with colorectal cancer at our institution between September 2000 and December 2003. These tumors had been histopathologically confirmed to be adenocarcinoma (Fig 1). The consecutive patients were all those who had undergone resection and in whom adenocarcinoma had been found. Sixty-one patients were male and 31 were female. Age at the time of surgery ranged from 42 to 87 years (mean age, 65 years ± 9 [standard deviation]).


Figure 1
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  		Figure 1: Flow diagram of the in vitro study of colorectal carcinomas with high-spatial-resolution 3D CISS MR imaging and histopathologic analysis.

 
All cancers were sporadic, and none of the patients had specific risk factors for colorectal cancer. Cancers were located in the rectum (n = 27), sigmoid colon (n = 22), ascending colon (n = 21), transverse colon (n = 14), cecum (n = 9), and descending colon (n = 3). Low anterior resection was performed in 21 patients; abdominoperineal resection, in six patients; and segmental resection, in 65 patients. Total mesorectal excision was not performed in patients with rectal cancer. No patient in this series underwent neoadjuvant therapy.

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 colorectal specimens were obtained initially. All specimens were imaged after fixation in formalin for 24–72 hours. No patient underwent MR imaging before surgery.

High-spatial-resolution 3D MR imaging was performed by using a 3D CISS sequence with the following parameters: 12.25/5.9 (repetition time msec/echo time msec), 70° flip angle, and two signals acquired. The acquisition matrix was 512 x 512 for an 80 x 80-mm field of view. Other imaging parameters included 47.5-mm slab thickness, 68 sections, and a 195 Hz/pixel bandwidth, which yielded 0.7-mm section thickness and 0.017-mm3 voxel size. Acquisition time was 14 minutes 14 seconds. The acquisition slab was oriented along the longitudinal axis of the resected colon and rectum so the entire tumor could be imaged. Slab thickness was not adjusted to tumor size, and one identical slab was used for all specimens. Tumor size ranged from 7 to 82 mm (mean, 35 mm ± 18).

Acquisition time was the time needed to acquire images of the segment of the colorectal specimen that included the tumor. One sequence was performed for each tumor. Colorectal specimen length ranged from 6.5 to 41.0 cm (mean, 16.9 cm ± 6.9).

The 3D data sets were postprocessed with image-processing software dedicated to Digital Imaging and Communications in Medicine images (OsiriX, version 2.4; Digital Imaging Unit, University Hospital of Geneva, Geneva, Switzerland) and commercially available software (VoxBlast; VayTek, Fairfield, Iowa). Surface rendering was performed to generate virtual MR endoscopic images of the colon and rectum.

Image Analysis
Two independent radiologists (I.Y., N.Y.; 16 and 6 years of experience, respectively, in detecting colorectal cancer on abdominal MR images) who were blinded to histopathologic findings interpreted MR images of each lesion. Histopathologic findings were used as the reference standard for analysis of MR findings. No feedback on the abnormal findings of previous studies was given during this study. When the radiologists disagreed about the findings, a diagnosis was made in consensus. Observers were blinded to all clinical, endoscopic, and imaging information; however, they were not blinded to the location and number of tumors because each tumor was imaged separately.

The 3D CISS MR findings were reviewed for signal intensity, continuity, and masses in the layers of the colorectal wall. We analyzed the signal intensity and contour of the tumor. We also analyzed intramural enlarged lymph nodes (>8 mm in diameter) attached to the tumor in the specimens. The depth of tumor penetration into the colorectal wall was assessed according to the tumor component of the International Union against Cancer Tumor-Node-Metastasis classification (2).

Observers used the following MR imaging criteria to determine the depth of involvement: (a) discrete mass(es) in the layers, (b) focal areas of abnormal signal intensity in the thickened layers, and (c) mucosal ulcerations with surrounding or underlying mass(es) (13). Observers used both the abnormal signal intensity and the configuration to differentiate between cancer and layers of the colorectal wall.

Concerning matching of the imaging findings with the histopathologic findings, we evaluated the deepest invasion area in each tumor on MR images and histopathologic sections (described below) separately to determine the tumor stage at imaging and histopathologic analysis separately. Thus, one (I.Y.) of the two radiologists involved in MR image interpretation matched the T stage at MR imaging with the T stage at histopathologic analysis for each tumor in the specimen.

The macroscopic type of the 96 tumors was assessed by examining virtual MR endoscopic images, and the macroscopic types were compared with the macroscopic findings at surgery. The tumors were classified into the following macroscopic types by means of visual inspection: type 0, superficial; type 1, protruding; type 2, ulcerative and localized; type 3, ulcerative and infiltrative; and type 4, diffusely infiltrative. Macroscopic type was based on the General Rules for Clinical and Pathological Studies on Cancer of the Colon, Rectum, and Anus published by the Japanese Society for Cancer of the Colon and Rectum (14).

Preparation and Examination of the Histopathologic Specimens: The Reference Standard
After MR imaging, the surgical specimen of the colon or rectum was sliced longitudinally so that it corresponded to the orientation of the MR images. The sliced specimens were embedded in paraffin and cut into 6-µm-thick slices with a microtome. The slices were then stained with hematoxylin-eosin, and an experienced pathologist (J.K., 15 years of experience with colorectal pathology) who was unaware of the MR imaging findings assessed the depth of carcinoma invasion of the colorectal wall.

Statistical Analysis
Sensitivity, specificity, and accuracy of high-spatial-resolution 3D CISS MR imaging in assessing tumor invasion of the colorectal wall in the 96 tumors were determined by means of comparison with the histopathologic findings. Spearman correlation coefficient analysis was used to compare (a) the T stage at 3D CISS MR imaging with that at histopathologic analysis and (b) the macroscopic type at virtual MR endoscopy with that at surgery. P < .05 indicated a significant difference. Confidence levels were not used in the analysis. All statistical tests were performed with a statistical software package (StatView, version 5.0; SAS Institute, Cary, NC). We did not use logistic regression analysis with generalized estimating equations to account for the clustering effects of multiple tumors in the same patient because each tumor was imaged separately in this series.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Signal Intensity Characteristics of Normal Colorectal Wall
High-spatial-resolution 3D CISS MR images showed that the surface material (including the adherent mucus) had high signal intensity and the mucosa (including the epithelial glands and lamina propria mucosae) and muscularis mucosae had low signal intensity (Fig 2). The submucosa had high signal intensity, and histopathologic examination revealed that it contained loose connective tissue, capillary vessels, and lymph channels. The submucosal fat tissue had low signal intensity. The high-spatial-resolution 3D CISS MR images enabled us to separate the muscularis propria into three layers: an inner circular muscle layer and an outer longitudinal muscle layer that were seen as two discrete low-signal-intensity structures separated by a thin high-signal-intensity band that corresponded to loose connective tissue. The subserosa, serosa, and adventitia appeared as a high-signal-intensity structure. On the basis of MR and histopathologic findings, we could not differentiate between the subserosa, serosa, and adventitia; therefore, we combined these structures into one group (Table 1).


Figure 2A
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  		Figure 2a: Images obtained at almost the same level in the same specimen. Any morphologic differences between the images are likely related to a difference between levels. ICM = inner circular muscle, ICT = intermuscular connective tissue, M = mucosa, m = mucus, OLM = outer longitudinal muscle, SM = submucosa, and SS = subserosa and serosa. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) clearly shows that the normal colorectal wall has four to six layers, which correspond well to the layers seen at histopathologic analysis. (b) Histopathologic slice of the normal colorectal wall shows the mucosa, submucosa, muscularis propria (inner circular muscle, intermuscular connective tissue, and outer longitudinal muscle), and subserosa and serosa. (Hematoxylin-eosin stain; original magnification, x3.3.)

 

Figure 2B
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  		Figure 2b: Images obtained at almost the same level in the same specimen. Any morphologic differences between the images are likely related to a difference between levels. ICM = inner circular muscle, ICT = intermuscular connective tissue, M = mucosa, m = mucus, OLM = outer longitudinal muscle, SM = submucosa, and SS = subserosa and serosa. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) clearly shows that the normal colorectal wall has four to six layers, which correspond well to the layers seen at histopathologic analysis. (b) Histopathologic slice of the normal colorectal wall shows the mucosa, submucosa, muscularis propria (inner circular muscle, intermuscular connective tissue, and outer longitudinal muscle), and subserosa and serosa. (Hematoxylin-eosin stain; original magnification, x3.3.)

 

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  		Table 1. Signal Intensity of Layers of Colorectal Wall on High-Spatial-Resolution 3D CISS MR Images

 
The high-spatial-resolution 3D CISS MR images clearly showed that the normal colorectal wall consisted of the following four to six layers that corresponded well to the layers of the colorectal wall observed at histopathologic analysis: mucosa (low signal intensity), submucosa (high signal intensity), inner circular muscle (low signal intensity), intermuscular connective tissue (high signal intensity), outer longitudinal muscle (low signal intensity), and subserosa, serosa, and adventitia (high signal intensity) (Fig 2, Table 1). Six layers were observed in 88 (96%) of the 92 specimens, while only four layers were observed in the remaining four (4%) specimens.

The intermuscular connective tissue within the muscularis propria was variable between individuals and between different areas of the colorectal wall. In areas where the intermuscular connective tissue was apparent, the colorectal wall appeared to consist of six layers. In areas where the intermuscular connective tissue was not apparent, the colorectal wall appeared to consist of four layers because the muscularis propria appeared as a single low-signal-intensity zone.

Evaluation of Colorectal Carcinoma Invasion
At histopathologic analysis, the 96 colorectal carcinomas in our series consisted of 19 carcinomas confined to the mucosa, 15 that had invaded the submucosa, 15 that had infiltrated the muscularis propria, and 47 that had penetrated the muscularis propria and extended into the subserosa, serosa, and adventitia. The signal intensity of the colorectal carcinomas depended on the histopathologic components of the tumor (Figs 3–6). The epithelial component of the tumor appeared to have low to intermediate signal intensity on the 3D CISS MR images.


Figure 3A
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  		Figure 3a: Colorectal carcinoma invading the submucosa. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) shows that an irregularly shaped low-signal-intensity tumor (arrows) contrasts with the high-signal-intensity submucosa. (b) Corresponding histopathologic slice shows carcinoma invading the submucosa (SM). MP = muscularis propria. (Hematoxylin-eosin stain; original magnification, x1.6.)

 

Figure 3B
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  		Figure 3b: Colorectal carcinoma invading the submucosa. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) shows that an irregularly shaped low-signal-intensity tumor (arrows) contrasts with the high-signal-intensity submucosa. (b) Corresponding histopathologic slice shows carcinoma invading the submucosa (SM). MP = muscularis propria. (Hematoxylin-eosin stain; original magnification, x1.6.)

 

Figure 4A
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  		Figure 4a: Colorectal carcinoma involving the muscularis propria. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) shows that an irregularly shaped tumor (arrows) has partially replaced the muscularis propria layer (arrowheads) but does not penetrate the muscularis propria layer. (b) Corresponding histopathologic slice shows carcinoma involving the muscularis propria (arrowheads). (Hematoxylin-eosin stain; original magnification, x1.3.)

 

Figure 4B
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  		Figure 4b: Colorectal carcinoma involving the muscularis propria. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) shows that an irregularly shaped tumor (arrows) has partially replaced the muscularis propria layer (arrowheads) but does not penetrate the muscularis propria layer. (b) Corresponding histopathologic slice shows carcinoma involving the muscularis propria (arrowheads). (Hematoxylin-eosin stain; original magnification, x1.3.)

 

Figure 5A
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  		Figure 5a: Colorectal carcinoma extending into the subserosa and serosa. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) shows a large irregularly shaped tumor completely disrupting all layers of the colorectal wall and extending into the subserosa and serosa (arrows). (b) Corresponding histopathologic slice shows carcinoma extending into the subserosa and serosa (arrows). (Hematoxylin-eosin stain; original magnification, x1.6.)

 

Figure 5B
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  		Figure 5b: Colorectal carcinoma extending into the subserosa and serosa. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) shows a large irregularly shaped tumor completely disrupting all layers of the colorectal wall and extending into the subserosa and serosa (arrows). (b) Corresponding histopathologic slice shows carcinoma extending into the subserosa and serosa (arrows). (Hematoxylin-eosin stain; original magnification, x1.6.)

 

Figure 6A
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  		Figure 6a: Colorectal carcinoma with lymph node metastasis. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) shows a large irregularly shaped tumor disrupting all layers of the colorectal wall and extending into the subserosa and serosa. Enlarged lymph nodes (arrows) are seen in the subserosal layer. (b) Corresponding histopathologic slice shows carcinoma extending into the subserosa and serosa and metastatic lymph nodes (arrows) in the subserosal layer. (Hematoxylin-eosin stain; original magnification, x1.2.)

 

Figure 6B
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  		Figure 6b: Colorectal carcinoma with lymph node metastasis. (a) Longitudinal high-spatial-resolution 3D CISS MR image (12.25/5.9, 70° flip angle) shows a large irregularly shaped tumor disrupting all layers of the colorectal wall and extending into the subserosa and serosa. Enlarged lymph nodes (arrows) are seen in the subserosal layer. (b) Corresponding histopathologic slice shows carcinoma extending into the subserosa and serosa and metastatic lymph nodes (arrows) in the subserosal layer. (Hematoxylin-eosin stain; original magnification, x1.2.)

 
We found that 3D CISS MR images were useful in assessing tumor invasion of the colorectal wall. Carcinomas confined to the mucosa (n = 19) appeared as low-signal-intensity discrete thickening in the mucosal layer. Carcinomas that had invaded the submucosa (n = 13) appeared as irregular low-signal-intensity mass lesions in contrast to high-signal-intensity submucosa (Fig 3). Carcinomas that had involved the muscularis propria (n = 13) appeared to have partially replaced the muscularis propria layer (Fig 4). Carcinomas that extended into the subserosa, serosa, and adventitia (n = 47) appeared as tumors that had completely disrupted the superficial and muscularis propria layers and had invaded the high-signal-intensity subserosa, serosa, and adventitia (Fig 5).

In 92 (96%) of the 96 colorectal carcinomas, the stage of mural invasion determined with high-spatial-resolution 3D CISS MR imaging accurately corresponded to that determined with histopathologic examination based on the International Union against Cancer Tumor-Node-Metastasis classification (Table 2). In four (4%) carcinomas, however, the stage of mural invasion as determined with MR images was higher than that determined with histopathologic examination. Two T1 carcinomas (invasion of the submucosa) were overestimated as T2 carcinomas (involvement of the muscularis propria), and two T2 carcinomas were overestimated as T3 carcinomas (involvement of the subserosa or adventitia) with 3D CISS MR imaging. In this series, there were no cases of underestimation of depth of mural invasion with 3D CISS MR imaging. In the colorectal specimens, T4 tumors directly invading other organs or structures could not be differentiated from T3 tumors because the colon or rectum and invaded organs were resected separately. Thus, we combined T3 and T4 tumors into one group (Table 2).


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  		Table 2. Comparison of High-Spatial-Resolution 3D CISS MR and Histopathologic Findings for Evaluating Depth of Colorectal Carcinoma Invasion

 
Spearman correlation coefficients were used to measure agreement between T stages at 3D CISS MR imaging and T stages at histopathologic analysis (r = 0.976, P < .001). The correspondence between T stages was excellent (slope, 0.983; intercept, –0.006).

High-spatial-resolution 3D CISS MR imaging also depicted intramural enlarged lymph nodes (>8 mm in diameter) attached to the tumor in 14 colorectal specimens, and histopathologic findings were positive for metastasis in all these specimens (Fig 6). The enlarged lymph nodes were clearly seen to have low signal intensity in the subserosal and adventitial layer on high-spatial-resolution 3D CISS MR images. There were 18 enlarged lymph nodes that ranged in size from 8.1 to 16.4 mm (mean size, 10.7 mm ± 2.4).

Intramural lymph nodes are lymph nodes on the colorectal wall that belong to the group of pericolic or perirectal lymph nodes. Regional lymph nodes include the pericolic or perirectal nodes and nodes along the course of a named vascular trunk. In this study, we analyzed only intramural enlarged lymph nodes attached to the tumor because we imaged the tumor and adjacent areas alone. This may be related to the fact that the specimens with enlarged lymph nodes on MR images were positive for metastasis at histopathologic analysis. However, we could not assess accuracy for the detection of lymph node metastases because most regional lymph nodes were resected separately at surgery.

Diagnostic Accuracy of High-Spatial-Resolution 3D CISS MR Imaging
MR imaging was used to correctly diagnose mucosal or submucosal invasion in all 96 colorectal carcinomas examined. Thus, both sensitivity and accuracy for diagnosis of mucosal or submucosal invasion were 100%, although specificity could not be evaluated (Table 3). MR imaging was used to correctly diagnose muscularis propria invasion in all 62 lesions in which it was present; however, a false-positive diagnosis was made in two of the 34 lesions in which there was no muscularis propria invasion. Thus, sensitivity, specificity, and accuracy in the detection of invasion of the muscularis propria were 100%, 94%, and 98%, respectively. MR imaging was used to correctly diagnose subserosal, serosal, or adventitial invasion in all 47 lesions in which it was present; however, it yielded a false-positive diagnosis in two of the 49 lesions in which there was no subserosal, serosal, or adventitial invasion. Thus, sensitivity, specificity, and accuracy in the detection of subserosal, serosal, or adventitial invasion were 100%, 96%, and 98%, respectively. In six (6%) of the 96 tumors, the observers did not agree on MR findings, and tumor invasion was assessed by means of consensus reading.


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  		Table 3. Diagnostic Accuracy of High-Spatial-Resolution 3D CISS MR Imaging for Evaluating Depth of Colorectal Carcinoma Invasion

 
Identification of Macroscopic Colorectal Carcinoma on Virtual MR Endoscopic Images
Macroscopic examination of the 96 colorectal carcinomas revealed that they consisted of 37 type 0 carcinomas (superficial), five type 1 carcinomas (protruding), 50 type 2 carcinomas (ulcerative and localized), and four type 3 carcinomas (ulcerative and infiltrative) (Table 4). There were no type 4 carcinomas (diffusely infiltrative) in our series.


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  		Table 4. Comparison of Virtual MR Endoscopic Image Findings and Macroscopic Findings for Evaluating Macroscopic Type of Colorectal Carcinoma

 
The macroscopic type of carcinoma (Table 4) diagnosed on the basis of virtual MR endoscopic images was confirmed to be the same as the macroscopic type of carcinoma diagnosed at surgery in 91 (95%) of the 96 carcinomas (Fig 7), and it differed from the actual macroscopic type of carcinoma that was diagnosed in the other five (5%) carcinomas. One type 0 carcinoma was misdiagnosed as type 1 carcinoma, two type 0 carcinomas were misdiagnosed as type 2 carcinomas, and two type 2 carcinomas were misdiagnosed as type 0 carcinomas.


Figure 7A
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  		Figure 7a: (a, c, e, g) Virtual MR endoscopic images and (b, d, f, h) macroscopic images in four types of colorectal carcinomas. (a, b) Superficial and flat carcinomas (type 0–IIa) (arrow). (c, d) Protruding carcinomas (type 1) (arrow). (e, f) Ulcerative and localized carcinomas (type 2) (arrow). (g, h) Ulcerative and infiltrative carcinomas (type 3) (arrow). The macroscopic findings at virtual MR endoscopy were confirmed when they were compared with macroscopic findings at surgery.

 

Figure 7B
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  		Figure 7b: (a, c, e, g) Virtual MR endoscopic images and (b, d, f, h) macroscopic images in four types of colorectal carcinomas. (a, b) Superficial and flat carcinomas (type 0–IIa) (arrow). (c, d) Protruding carcinomas (type 1) (arrow). (e, f) Ulcerative and localized carcinomas (type 2) (arrow). (g, h) Ulcerative and infiltrative carcinomas (type 3) (arrow). The macroscopic findings at virtual MR endoscopy were confirmed when they were compared with macroscopic findings at surgery.

 

Figure 7C
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  		Figure 7c: (a, c, e, g) Virtual MR endoscopic images and (b, d, f, h) macroscopic images in four types of colorectal carcinomas. (a, b) Superficial and flat carcinomas (type 0–IIa) (arrow). (c, d) Protruding carcinomas (type 1) (arrow). (e, f) Ulcerative and localized carcinomas (type 2) (arrow). (g, h) Ulcerative and infiltrative carcinomas (type 3) (arrow). The macroscopic findings at virtual MR endoscopy were confirmed when they were compared with macroscopic findings at surgery.

 

Figure 7D
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  		Figure 7d: (a, c, e, g) Virtual MR endoscopic images and (b, d, f, h) macroscopic images in four types of colorectal carcinomas. (a, b) Superficial and flat carcinomas (type 0–IIa) (arrow). (c, d) Protruding carcinomas (type 1) (arrow). (e, f) Ulcerative and localized carcinomas (type 2) (arrow). (g, h) Ulcerative and infiltrative carcinomas (type 3) (arrow). The macroscopic findings at virtual MR endoscopy were confirmed when they were compared with macroscopic findings at surgery.

 

Figure 7E
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  		Figure 7e: (a, c, e, g) Virtual MR endoscopic images and (b, d, f, h) macroscopic images in four types of colorectal carcinomas. (a, b) Superficial and flat carcinomas (type 0–IIa) (arrow). (c, d) Protruding carcinomas (type 1) (arrow). (e, f) Ulcerative and localized carcinomas (type 2) (arrow). (g, h) Ulcerative and infiltrative carcinomas (type 3) (arrow). The macroscopic findings at virtual MR endoscopy were confirmed when they were compared with macroscopic findings at surgery.

 

Figure 7F
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  		Figure 7f: (a, c, e, g) Virtual MR endoscopic images and (b, d, f, h) macroscopic images in four types of colorectal carcinomas. (a, b) Superficial and flat carcinomas (type 0–IIa) (arrow). (c, d) Protruding carcinomas (type 1) (arrow). (e, f) Ulcerative and localized carcinomas (type 2) (arrow). (g, h) Ulcerative and infiltrative carcinomas (type 3) (arrow). The macroscopic findings at virtual MR endoscopy were confirmed when they were compared with macroscopic findings at surgery.

 

Figure 7G
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  		Figure 7g: (a, c, e, g) Virtual MR endoscopic images and (b, d, f, h) macroscopic images in four types of colorectal carcinomas. (a, b) Superficial and flat carcinomas (type 0–IIa) (arrow). (c, d) Protruding carcinomas (type 1) (arrow). (e, f) Ulcerative and localized carcinomas (type 2) (arrow). (g, h) Ulcerative and infiltrative carcinomas (type 3) (arrow). The macroscopic findings at virtual MR endoscopy were confirmed when they were compared with macroscopic findings at surgery.

 

Figure 7H
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  		Figure 7h: (a, c, e, g) Virtual MR endoscopic images and (b, d, f, h) macroscopic images in four types of colorectal carcinomas. (a, b) Superficial and flat carcinomas (type 0–IIa) (arrow). (c, d) Protruding carcinomas (type 1) (arrow). (e, f) Ulcerative and localized carcinomas (type 2) (arrow). (g, h) Ulcerative and infiltrative carcinomas (type 3) (arrow). The macroscopic findings at virtual MR endoscopy were confirmed when they were compared with macroscopic findings at surgery.

 
Spearman correlation coefficients were used to assess agreement between macroscopic type at virtual MR endoscopy and macroscopic type at surgery (r = 0.916, P < .001). The correspondence was excellent (slope, 0.920; intercept, 0.088).


   DISCUSSION
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 
Our findings show that high-spatial-resolution 3D CISS MR imaging clearly depicts the normal colorectal wall as consisting of four to six layers that correspond well to the actual layers of the colorectal wall seen at histopathologic analysis. Previous studies have shown that conventional T2-weighted spin-echo MR imaging depicts three to five layers of the colorectal wall (8,9). Our results show that high-spatial-resolution 3D CISS MR imaging clearly depicts the actual layers of the colorectal wall seen at histopathologic analysis.

Our findings show that high-spatial-resolution 3D CISS MR imaging correctly depicted the depth of invasion of the colorectal wall for 92 (96%) of the 96 colorectal carcinomas studied. Although the depth of invasion was incorrectly assessed in four (4%) carcinomas, sensitivity, specificity, and accuracy of high-spatial-resolution 3D CISS MR imaging in determining the depth of invasion of the colorectal wall were 100%, 94%–96%, and 98%–100%, respectively. Thus, high-spatial-resolution 3D CISS MR imaging was found to have a high degree of accuracy in the in vitro evaluation of the depth of invasion by colorectal carcinoma.

In vivo endorectal MR imaging has been used to stage rectal cancer (15–17). Study findings have shown that conventional spin-echo MR imaging with endorectal coils allows T staging of rectal cancer with an accuracy of 71%–91% (10,15,18). Akin et al (17) also reported that endorectal MR imaging was histopathologically accurate for T staging of rectal cancer in 17 (85%) of 20 patients. MR imaging with phased-array and endorectal coils has been used for local staging of rectal cancer (19–21). On the basis of a meta-analysis in which 90 articles published between 1985 and 2002 were used, Bipat et al (22) reported that MR imaging for T staging of rectal cancer had a sensitivity of between 74% and 94% and a specificity of between 69% and 96%. The previous reports suggested that conventional MR imaging might have had substantial limitations in T staging of rectal cancer (9,10,22). Thus, more accurate methods are needed.

There are substantial differences in the management of rectal cancers and colon cancers and subsequent differences in the imaging requirements. This is evident in patients with more advanced cancers. In patients with advanced rectal cancers, the role of imaging is more extensive, and accurate staging should include consideration of the distance between the tumor or tumor deposit and the mesorectal fascia. In patients with advanced colon cancers, the role of imaging may be more limited (23). However, in patients with cancers detected at an earlier stage, determining the depth of cancer invasion with use of imaging is important for both rectal and colon cancers. Knowledge of the correct depth of invasion is necessary to select the most appropriate therapy—such as polypectomy, endoscopic mucosal resection, local excision, or radical operation—for rectal and colon cancers (1,2,24,25).

Our findings have also shown that the same 3D CISS imaging data set can be used to generate virtual MR endoscopic images. Furthermore, the virtual MR endoscopic images clearly showed the macroscopic type of carcinoma found at surgery. Knowledge of the gross configuration of the carcinoma and the correct depth of invasion is essential to select the most appropriate therapy for colorectal carcinoma (1,2,24,25). Virtual endoscopic MR imaging has been used to detect colorectal carcinoma (26–29), and Luboldt et al (26) found that MR colonography with virtual endoscopic viewing had high diagnostic accuracy in the detection of colorectal mass lesions larger than 10 mm in diameter. High-spatial-resolution 3D CISS MR imaging, which has higher spatial resolution, is expected to be a useful method in the detection and macroscopic evaluation of colorectal carcinomas.

A limitation of our study is that the specimens were imaged after they were fixed in formalin. Imai et al (30) found that the signal intensity of the muscularis propria on T2-weighted spin-echo MR images of the colorectal wall was slightly higher in fresh specimens than in formalin-fixed specimens and that the contrast between the submucosa and the muscularis propria was slightly lower on images of fresh specimens. Auh et al (31) found no correlation between signal intensity on spin-echo MR images of the stomach wall and duration of formalin fixation. Yamada et al (32) also reported that there was no substantial difference between the signal intensities of fresh specimens and those of formalin-fixed specimens on T2-weighted images of the esophageal wall. The results of these two studies in which T2-weighted spin-echo images were used have shown that formalin fixation has no substantial effect on signal intensity or tissue contrast. The 3D CISS images are essentially T2-weighted images, although they are obtained with a gradient-echo–based sequence. Thus, the findings in our study might be applicable to high-spatial-resolution 3D CISS MR images of in vivo specimens and formalin-fixed specimens.

Another limitation of our study is that we performed only 3D CISS imaging and compared these findings with histopathologic findings; thus, this sequence was not compared with T2-weighted spin-echo or fast spin-echo sequences. Conventional spin-echo T2-weighted images of colorectal cancers have been the subject of numerous reports, including reports of in vitro and in vivo studies, which have described the range of diagnostic accuracy. Thus, in our study, we compared 3D CISS MR imaging with histopathologic analysis and compared the diagnostic accuracy of this imaging technique with that of conventional spin-echo T2-weighted imaging as reported in the literature.

Finally, we used a dedicated coil and long acquisition times to obtain images of specimens fixed in formalin; therefore, our findings cannot be directly extrapolated to an in vivo setting. Thus, 3D CISS MR imaging might be applicable to clinical practice only after in vivo validation of this technique.

In conclusion, our findings show that in vitro high-spatial-resolution 3D CISS MR imaging clearly depicts the internal architecture of the colorectal wall and has high diagnostic accuracy in the evaluation of mural invasion and the macroscopic features of colorectal carcinomas. Thus, high-spatial-resolution 3D CISS MR imaging may enable preoperative histopathologic staging and morphologic evaluation of colorectal carcinomas after in vivo evaluation of this technique.

Practical application: High-spatial-resolution 3D CISS MR imaging may be a new tool for accurate preoperative histopathologic staging and morphologic evaluation of colorectal carcinoma after in vivo validation of this technique.


   ADVANCES IN KNOWLEDGE
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 


   IMPLICATION FOR PATIENT CARE
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References
 


   FOOTNOTES
 

Abbreviations: CISS = constructive interference in steady state • 3D = three-dimensional

Guarantor of integrity of entire study, I.Y.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, I.Y., N.Y., A.T.; clinical studies, I.Y., S.O., M.E., K.S.; experimental studies, I.Y., N.Y., A.T., J.K.; statistical analysis, I.Y., J.K.; and manuscript editing, I.Y.

Authors stated no financial relationship to disclose.


   References
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RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE...
 References
 

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