Chin J Radiol 2003; 28: 269-275 269 Application of Magnetic Resonance Images in Gastrointestinal Malignancies SHENG-LAN YU 1 YUK-MING TSANG 1 PO-CHIN LIANG 1 HUNG-JUNG WANG 1 CHIEN-YAO HSU 1 TA-CHENG WEI 2 Departments of Medical Imaging 1, Surgery 2, National Taiwan University Hospital Thirty three patients, who were previously documented to have gastric, duodenal or colorectal malignancies by endoscopy and biopsy, underwent magnetic resonance imaging (MRI) to evaluate the clinical usefulness of MRI on assessing depth of invasion, regional lymphadenopathy and hepatic metastasis. Most of these patients had undergone either barium or computed tomgraphy (CT) studies within one week before the MR imaging. The MRI, CT, and operative findings including tumor extension, extraserosal invasion, regional lymph nodes and regional or distant metastases were compared. The results showed that MRI provided advantages over CT for determining local invasion because of high tissue contrast and multiplanar imaging capacity. In addition, MRI provided high quality images in the patient with gastric outlet or colonic obstruction that the retained barium might prohibit subsequent CT scan. In such situations, barium studies only showed the obstruction; however, the lesion would be better depicted by MRI. Furthermore, MRI was comparable to CT in showing regional lymphadenopathy and hepatic metastasis. As a result, it is suggested that MRI has the potential to replace the combination of barium study and CT for preoperative staging of gastrointestinal malignancies in the situation when the latters may not be performed optimally. Key words: GI tract; Malignancies; Megnetic resonance imaging Reprint requests to: Dr. Yuk-Ming Tsang Departments of Medical Imaging, National Taiwan University Hospital. No. 7, Chung Shan S Road, Taipei 100, Taiwan, R.O.C. Gastric and colorectal cancers are common gastrointestinal malignancies for both men and women in Taiwan. The most important determinants of survival are the presence of hepatic metastasis, involvement of the lymph nodes and extent of the tumor through the bowel wall. A complete pre-operative evaluation for gastric and colorectal cancer usually consists of endoscopy with biopsy for tissue diagnosis, barium study for locating the tumor and a topographic depiction of the extent, and computed tomgraphy (CT) for staging. However, LGI study may cause bowel perforation after an endoscopic biopsy. Besides, barium and CT study may interfere with each other, especially when CT is done after a barium study. Thus, a complete preoperative assessment may be time-consuming. The purpose of this study is to examine whether the preoperative staging with a single magnetic resonance imaging (MRI) will be more accurate and efficient than that combining CT and barium studies. Clinical materials and method From March 1999 to March 2000, we had 33 patients undergoing MRI study because of newly diagnosed, untreated gastrointestinal malignancies 13 cases of gastric cancer, 1 case of duodenal cancer and 19 cases of colorectal cancer. Of these, 17 of the patients were female, and 16 were male. The preoperative diagnosis was established with endoscopy or a barium study, and subsequent examinations were conducted for a complete preoperative staging. Among these patients, 11 received MR and CT but no barium studies, while 10 without CT and 12 with all these 3 studies. Imaging methods Among the cases of gastric or duodenal malignancies, patients who underwent an 8-hour fasting drank 500ml water prior to MRI as an oral contrast agent. To all these cases, an intramuscular injection of 20mg of Buscopan (Boehringer International, Ingelheim,
270 MRI in GI malignancies Germany) was also given 10 minutes before examination in order to slow down peristalsis [1]. For patients with colorectal malignancies, standard bowel preparation, including a clear liquid diet, administration of 4 tabs of Bisacodyl (5mg) at the night before MR scanning, were carried out for all patients. One amp of Buscopan was given intramuscularly prior to MRI scanning. After the patients lying inside the MRI magnet bore, about 500-700 ml of air was insufflated per rectum. MR imaging protocols All the images were obtained from a 1.5T Magnetom Vision Plus whole body imager (Seimens AD, Erlangen, Germany). The imaging protocols included [2, 3]: 1. 2D FLASH (TR = 93.5~166.2 msec; TE = 4.1/1 msec) and True-FISP (TR = 6.3 msec; TE = 3.0/1 msec) sequences in coronal sections with a body coil (FOV = 45cm; section thickness = 5 mm; gap = 1.5mm; NEX = 1), scanning from the diaphragm to the anus for localization in a single breath-hold. 2. 2D FLASH and True-FISP sequences in axial and sagittal planes with a body array (FOV = 30 x 30 cm in colorectal lesions, 33~35 cm in gastroduodenal lesions; section thickness = 5 mm; gap = 1.5mm) for the local lesion. 3. Axial T2-weighted HASTE (half-fourier acquisition single shot turbo spin echo) sequence with a body array (TR = 4.4 msec; TE = 64.0/1 msec; FOV = 25 30 cm; section thickness = 8 mm) for the liver. 4. Post-contrast 2D FLASH with a body array in axial, coronal and sagittal planes for the local lesion and liver (in axial plane). 5. In the cases of gastroduodenal lesions, supine, prone, right or left lateral decubitus were needed according to the patient's lesion site which was usually available as most of these patients had undergone endoscopy or UGI barium study. 6. If necessary, a magnified view with small FOV was performed. CT imaging protocol CT studies were performed with spiral or electron beam CT scanners. In the cases of gastric or duodenal malignancies, the patients fasted at least 4 hours before CT examination, then drank 500 ml water and were administrated 20 mg Buscopan intramuscularly immediately before the study. The scanned area was from the hepatic dome to the iliac crest with 8-mmthickness sections for the pre-contrast images and 5 mm for the post-contrast ones. To the cases of colorectal malignancies, the patients drank 1000 ml and 500 ml diluted Urographin syrup 8 hours and 10 minutes before the CT studies. The entire abdomen and pelvis were scanned from the hepatic dome to the anus with 8-mm- thickness sections. Barium study UGI or LGI studies were performed with routine double contrast technique using EZ-HD (E-Z-EM, Inc. Westbury, NY.). Image evaluation All the images were reviewed to determine the 1a 1b Figure 1. A 44 y/o male with abdominal distension. a. UGI showed gastric outlet obstruction with marked retention of barium in stomach and too much gastric juice that obscured the lesion. Detail evaluation was impossible. CT was tried next day and was given up due to too much artifacts caused by residual barium; b. Coronal True-FISP MR imaging showed huge infiltrative tumor at distal antrum (arrow) causing outlet obstruction. Extraserosal invasion (arrowheads) of this lesion was identified.
MRI in GI malignancies 271 extent of the lesion and the presence of extraserosal invasion, regional lymph node enlargement, and hepatic metastasis [4]. Extraserosal invasion was defined as spicules or strandings larger than 5mm, projecting from the profile of the GI tube. Lymph nodes measuring more than 1cm in diameter or a cluster of more than 3 nodes which equal to or less than 1 cm were considered abnormal lymphadenopathy [5]. Hepatic metastases were considered as focal lesion in liver excluding cysts or hemangiomas [6]. RESULTS Twenty-eight of 33 patients underwent operation after MRI study; 2 cases of advanced gastric cancer and 3 cases of gastric or duodenal lymphoma were not operated upon because the formers were unresectable and the latters received chemotherapy. The image findings were compared with the operative findings as well as the pathological reports. 1. Extent of the lesion: To those cases of gastric outlet obstruction caused by gastroduodenal lesions, marked retention of barium and gastric juice obscured the lesion in UGI study. It not only made the detail evaluation of UGI study impossible but also generated much artifact in the subsequent CT (Fig. 1). To those cases of colorectal cancer, the LGI studies were not optimal for two of the 19 patients due to nearly total obstruction at the lesion sites. The barium suspension could not fill the colon above the lesion; neither was the colofibroscopy able to pass through. As a result, the CT of these two cases only demonstrated the lesions in the axial plane. Hence, the extent of the lesions was poorly defined by these studies. On the other hand, the MR imaging showed the extent of the lesions in all of the patients directly (Fig. 2 and 3). With the use of i.v. contrast medium, the depth of invasion could be estimated more easily and it also served to distinguish a true lesion, which could be enhanced, from fecal material (Fig. 2) 2. Extraserosal invasion: In table 3 and 4, histopathologically proved extraserosal invasion was found in 5 patients (60%) with gastric adenocarcinoma and 16 (84%) with colorectal cancer. The sensitivity, specificity and accuracy of CT and MR in detecting extraserosal invasion were compared with operative finding in Table 1 and 2. Table 1. Assessment of extraserosal invasion of gastric adenocarcinoma with CT, MR imaging and operative finding CT (n=5) 0.33 (1/3) 1.00 (2/2) 0.60 (3/5) MR (n=8) 0.60 (3/5) 0.67 (2/3) 0.63 (5/8) Operative finding (n=8) 0.60 (3/5) 1.00 (3/3) 0.75 (6/8) Table 2. Assessment of extraserosal invasion of colorectal cancer with CT, MR imaging and operative finding CT (n=13) 0.75 (9/12) 1.00 (1/1) 0.77 (10/13) MR (n=19) 0.88 (14/16) 0.67 (2/3) 0.84 (16/19) Operative finding (n=19) 0.69 (11/16) 0.67 (2/3) 0.68 (13/19) 2a 2b Figure 2. A 72 y/o male patient with descending colon cancer. a. Double contrast of barium enema study revealed a long segment apple-core lesion (double arrows) with nodular and ulcerated surface at distal descending colon; b. Coronal 2D FLASH T1 weighted fat-suppressed images before (left) and after (right) Gd-DTPA showed prominent enhancement to the tumor (arrow) at the distal descending colon. It served to exclude fecal material (arrowhead) in sigmoid colon as a lesion.
272 MRI in GI malignancies 3. Regional lymph node involvement: Four of 10 patients with gastric adenocarcinoma were proved to have regional lymph node metastasis, and so were 7 of 17 with colorectal cancer. The sensitivity, specificity and accuracy of CT and MR in detecting regional lymph node involvement were compared with operative findings (See in Table 3 and 4). 4. Hepatic metastasis: There was only one case of hepatic metastasis from gastric adenocarcinoma noted in both preoperative MR and CT. Two cases of colorectal cancer were demonstrated by the preoperative MR study and confirmed by the follow-up CT. However, they were not detected in the preoperative CT images. DISCUSSION Conventionally, the MRI imaging of gastrointestinal disease does not generate high-quality images due to varying distensibility of the gastric wall and artifacts caused by peristalsis and respiration. However, recent advances in MR imaging technique have overcome these limitations [1, 2, 3]. Fast imaging techniques is capable of imaging the gastrointestinal tract in a single breath-hold after administration of anticholinergic agent to slow down the peristalsis and distension by water or air. In this study, good images of the gastrointestinal tract with little motion artifact were obtained in all cases. MR is an excellent imaging tool to differentiate mucosal from submucosal lesions because of its multiplanar imaging ability (Fig. 4) and clear delineation of the mucosa after Gadolinium contrast enhancement (Fig. 5) [7]. In our study, submucosal lesions (lymphomas in our study) can be easily distinguished from gastric adenocarcinomas in MR images. In contrast, they would be otherwise difficult to differen- Table 3. Assessment of regional lymph node involvement of gastric adenocarcinoma with CT, MR imaging and operative finding CT (n=5) 0.00 (0/3) 1.00 (2/2) 0.40 (2/5) MR (n=8) 0.00 (0/4) 0.75 (3/4) 0.38 (3/8) Operative finding (n=8) 0.50 (2/4 1.00 (4/4) 0.75 (6/8) Table 4. Assessment of regional lymph node involvement of colorectal cancer with CT, MR imaging and operative finding CT (n=13) 0.67 (4/6) 0.29 (2/7) 0.46 (6/13) MR (n=19) 0.67 (6/9) 0.40 (4/10) 0.53 (10/19) Operative finding (n=19) 0.44 (4/9) 0.60 (6/10) 0.53 (10/19) 3a 3b 3c Figure 3. A 64 y/o male patient with rectal cancer. a. Double contrast study showed annular stenosis (double arrows) with apple core appearance at the distal rectum. The CT scan after the LGI study demonstrated large amount of artifacts caused by retained barium (not shown), obscuring the detail of abdominal structure; b. c. Post-contrast T1 weighted 2D FLASH fat-suppressed images in axial b. and coronal c. views showed eccentric wall thickening (large arrow) at the mid-low rectum. The lumen was nearly totally obstructed and pushed to the right and posteriorily. b. There was remarkable lateral extension of the tumor, touching the left pelvic sidewall. Lymphadenopathy (arrowhead) was noted at the perirectal space.
MRI in GI malignancies 273 tiate from adenocarcinoma in routine axial abdominal CT. The accuracy of detection of extraserosal invasion and regional lymphadenopathy in gastric adenocarcinoma with CT or MRI was not satisfactory in our study as we only relied on size as a criterion. Nevertheless, many cases in our study showed that Figure 4. A 33 y/o female with advanced gastric cancer. left: UGI series in supine position showed a plate-like lesion with uneven surface at greater curvature side of body and antrum (arrow). Right: Coronal True-FISP MR imaging showed the lesion and a clear interface with the other adjacent intestinal loops (arrowhead). No extraserosal invasion was found after operation. Note the superior tissue contrast between the stomach and its clear interface with adjacent intestinal loop. Note also the excellent contrast between the lesion and the gastric juice so that the unevenness of the surface and the extent of invasion could be estimated more precisely. MRI was superior to combined CT and UGI studies to evaluate tumor extension and extraserosal invasion. This study showed that MR imaging was highly appreciated to patients with gastric cancer having gastric outlet obstruction (Fig. 1). The UGI study was suboptimal due to poor barium coating. Moreover, the barium of previous UGI did not pass through the obstruction site and the dense artifacts so produced interfered with subsequent CT examination. In this situation, MRI smoothly circumvented such drawback and was able to provide satisfactory demonstration of the extent of the disease. In colorectal cancer, our study showed that MR imaging was better than the combination of LGI and CT in determining the longitudinal extent of colorectal cancer (Fig. 2). In the evaluation of tumor penetration beyond the muscularis propria of the colonic wall, MR appeared to be more sensitive than CT imaging. Because of low incidence of negative extraserosal invasion in this series, the specificity of both examinations may not be valid. By comparing CT with the operative findings, however, the accuracy of detecting extraserosal invasion resulting from MR was still higher. The issue deserves further study so that a larger case number may reflect the actual potential of MRI s capability in evaluating depth invasion. MR imaging accurately detected and staged rectosigmoid cancer and had better results in these areas than in the other regions of the colon [1, 5]. It is because the rectosigmoid is relatively fixed in the pelvis. Furthermore, MR imaging performed in the 5a Figure 5. A 81 y/o female with lymphoma. a. Contrast enhanced CT showed circumferential thickening (arrow) at the 2nd portion of the duodenum but the relationship with the pancreatic head was not clear. b. Post-contrast coronal T1 weighted 2D FLASH MR imaging revealed that the lesion confines only to the duodenum, and in the submucosal layer, with intact mucosa (arrowhead) which was well enhanced. There was neither invasion to the pancreatic head nor commonbile duct. 5b
274 MRI in GI malignancies coronal plane with gadolinium enhancement is very useful for detecting tumor involvement of the levator ani muscles. This is very important for a complete preoperative assessment; an anterior resection should not be performed and an AP resection is required if the levator ani muscles are involved. This makes MR a better imaging modality than conventional axial CT in evaluating of colorectal cancer. In the assessment of regional lymph node involvement in colorectal cancers, both CT and MR imaging had low sensitivity and specificity [4]. The operative finding was neither sensitive nor specific for regional lymph nodes assessment. The reason may be that some enlarged lymph nodes are only histologically reactive, but not metastatic. Moreover, lymph nodes may be abnormal in pathology although their size would be considered as normal in MRI and CT. Therefore, the low sensitivity of CT and MR imaging may simply reflect an inherent inability to detect microscopic nodal involvement. Owing to the small number of cases of liver metastasis in our study, it is not significant to tell which one is better for detecting liver metastasis. In two cases of this series, however, the preoperative CT did not detect the liver metastasis, of which the MR imaging picked up the hepatic lesions. Previous reports showed similar accuracies of CT and MR in the detection of liver metastasis, but some reported that MR imaging is superior to CT [6, 8]. There are some minor drawbacks in MR imaging. Owing to the long examination time (about 20-25 seconds per single breath-hold) required by MR imaging, more motion artifact may occur, especially for elderly patients who cannot hold their breath properly. Considering these cases of colorectal cancer, air insufflation was attempted in every patient, and the long examination time of MR may lead to lower patient tolerance and inadequate colonic distension. Nevertheless, the scanning time of MR imaging is comparable to that of the double contrast barium study. Besides, MR imaging is more tolerable than the double contrast barium study. In contrast, CT scanning is faster and may lower the motion artifact in less cooperative patients. In summary, the multiplanar imaging ability of MR offers special advantages in evaluating local tumor extent. Simple True-FISP and 2D FLASH sequences with and without intravenous contrast enhancement are enough to clarify the lesion. Contrast enhancement could help to differentiate tumor from fecal material. Furthermore, MR imaging reveals the precise anatomic location of the tumor, which is essential for a surgery and is traditionally achieved by a barium study. As a result, it is suggested that CT and barium study could be replaced by a single MR study so that the preoperative assessment would be more efficient and accurate. SUMMARY This is a preliminary study to evaluate the possibility of using MRI for pre-operative evaluation of gastrointestinal malignancies. It shows that MR imaging is more accurate than the combination of barium study and CT in defining the longitudinal extent and extraserosal invasion in gastrointestinal malignancies. Both CT and MR imaging exhibit relatively low accuracies in assessment of regional lymph node involvement. MR imaging seems to be more sensitive in detecting liver metastasis but it should be examined by further study. A single MRI may replace CT and barium study in defining local tumor extent, anatomic location of the tumor, and hepatic metastasis for the preoperative staging in the situation when the latters may not be performed satisfactorily. REFERENCE 1. Goldberg HI, Thoeni RF. MRI of the gastrointestinal tract. Radiol Clin North Am 1987; 27: 805-812 2. Chien D, Atkinson DJ, Edelman PR. Strategies to improve contrast in turboflash imaging: recorded phase encoding and k-space segmentation. Journal of Magnetic Resonance Imaging 1991; 1: 63-70 3. Saini S, Stark DD, Rzedzian RR, et al. Forty-millisecond MR imaging of the abdomen at 2.0 T. Radiology 1989; 173: 111-116 4. Zerhouni EA, Rutter C, Hamilton SR, et al. CT and MR imaging in the staging of colorectal carcinoma: report of the Radiology Diagnostic Oncology Group II. Radiology 1996; 200: 443-451 5. Thoeni RF. Colorectal cancer: radiologic staging. Radiol Clin of North Am 1997; 35: 457-485 6. Reinig JW, Dwyer AJ, Miller DL, et al. Liver metastasis detection: comparative sensitivities of MR imaging and CT scanning. Radiology 1987; 162: 43-47 7. Kang BC, Kim JH, Kim KW, et al. Value of the dynamic and delayed MR sequence with Gd-DTPA in the T- staging of stomach cancer: correlation with the histopathology. Abdominal Imaging 2000; 25: 14-24 8. Schwartz LH. Advances in cross-sectional imaging of colorectal cancer. Seminars in Oncology 1999; 26: 569-76
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