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Gastrointestinal Imaging |
1 From the Department of Radiology, Kumamoto University Hospital, 1-1-1 Honjo, Kumamoto City 860-0811, Japan. Received December 24, 1997; revision requested March 24, 1998; final revision received November 24; accepted March 2, 1999. Address reprint requests to Y.Y. (e-mail: yama@kaiju.medic.kumamoto-u.ac.jp).
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Abstract |
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MATERIALS AND METHODS: Fifty-seven patients (37 men, 20 women aged 42–28 years) suspected of having pancreatic adenocarcinoma were examined. The final diagnosis was confirmed at surgery to be pancreatic cancer in 31 patients; the other 26 patients were deemed not to have pancreatic cancer. All patients underwent both CT and MR imaging (turbo spin-echo and fast low-angle shot) studies. Image quality and pancreatic enhancement were subjectively evaluated. All CT scans and MR images were assessed by two independent observers by using a five-point scale for the detection of tumor and of invasion into the peripancreatic tissue, portal vein, and/or peripancreatic artery. Receiver operating characteristic curves for CT and MR imaging were analyzed.
RESULTS: At visual analysis, pancreatic enhancement at CT and at MR imaging was comparable, but depiction of vessels was superior at helical CT. Detectability of tumor was comparable. Helical CT was significantly superior to MR imaging in diagnostic imaging of invasion into the peripancreatic tissue, portal vein, and/or peripancreatic artery (P < .01).
CONCLUSION: Thin-section dynamic CT is more sensitive than MR imaging for detection of peripancreatic and vascular invasion in patients with pancreatic cancer.
Index terms: Computed tomography (CT), comparative studies, 77.12111, 77.12112, 77.12115, 77.12118 • Magnetic resonance (MR), comparative studies, 77.121411, 77.121415, 77.121416, 77.12143 • Pancreas, CT, 77.12111, 77.12112, 77.12115, 77.12118 • Pancreas, MR, 77.121411, 77.121415, 77.121416, 77.12143 • Pancreas, neoplasms, 77.291, 77.321, 77.33 • Receiver operating characteristic curve (ROC)
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Among the several potential advantages of MR imaging are high tissue contrast, which might increase the conspicuity of the pancreatic lesions, and the option to manipulate pulse sequence parameters to improve depiction of structures such as blood vessels and the pancreas (10–16).
Although the findings of studies (10–12,14–17) suggest the superiority of MR imaging, especially dynamic imaging, over CT in the assessment of pancreatic neoplasms, to our knowledge, this superiority has not been recognized in clinical situations: With the exception of a report by Ichikawa et al (11), in which helical CT was used, all prospective studies were conducted before helical CT became widely available (14–16). Thus, the goal of this study was to compare, by means of receiver operating characteristic (ROC) analysis, technically optimized thin-section helical CT with technically optimized MR imaging for sensitivity in the detection of pancreatic adenocarcinoma and for accuracy in assessing vascular invasion or invasion into peripancreatic tissue.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The preoperative criteria for definitely nonresectable cancer included the presence of distant metastasis, multiple liver metastases, peritoneal dissemination with massive ascites, and involvement of the neighboring major vascular system (ie, encasement of the celiac axis and superior mesenteric artery). Involvement of the superior mesenteric vein or main portal vein was not a contraindication to resectability, because resection of tumor and reconstruction of the portal venous system could be performed, if necessary. If the tumor was nonresectable, surgical biopsy followed by bypass surgery (ie, gastrojejunostomy combined with biliary-jejunostomy) was performed.
Histopathologic evaluation included the notation of the size, location, appearance, and histologic features of the mass and associated complications (eg, pancreatitis). When a pancreatic tumor was completely resected, the pathologic results were used as the standard of reference for diagnosis. When the lesion was nonresectable, the operative findings were used as the standard of reference. When the mass was not resected, the pathologist indicated the histologic nature of the tissue sampled at biopsy. Surgeons indicated whether a mass was present at palpation and at intraoperative US. We could not spatially localize the pathologic conditions of the actual vessels and of the actual peripancreatic fat to compare them with the imaging findings. Intraoperative US was performed to confirm vascular encasement by the tumor. Manual palpation of a pancreatic mass fixed to retropancreatic vessels or structures, with intraoperative US–based confirmation of vascular encasement, was considered adequate surgical confirmation of extrapancreatic invasion and therefore of nonresectability. No attempt was made at surgery to visualize every liver lesion depicted on the images. Infiltration of the pancreatic capsule was assessed, as was invasion into the surgical resection margins.
Imaging Techniques
CT protocol.—All CT examinations were carried out by using a helical CT scanner (CT HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis). Each patient was asked to drink 300 mL of water to fill the duodenum. We did not use any other oral contrast material. For the intravenous contrast material, 300 mg of iodine per milliliter of iopamidol (Iopamiron 300; Schering, Osaka, Japan) was injected at a rate of 3 mL/sec for 30 seconds (total dose, 2 mL/kg). A 20-gauge needle was positioned in a medial antecubital vein, and the rate of flow was controlled with a power injector. After nonenhanced CT scanning, cephalocaudal scanning through the pancreatic region was begun 35 seconds (early phase), 70 seconds (portal venous phase), and 240 seconds after the start of the contrast material injection.
For thin-section helical CT imaging of the pancreas, the examination began at the level of the splenic hilum just cephalad to the pancreatic tail. The position of the pancreas was determined by obtaining axial images of the entire pancreas before the administration of contrast material (ie, precontrast images). Patients were prepared for the breath hold with three coached, deep respiratory excursions before scanning. In one breath hold, an area of 7 or 8 cm was scanned; this coverage included the pancreas in all patients.
Helical CT scanning during the early phase and portal venous phase was performed with a breath-hold technique in a 1 second per gantry rotation with a table feed of 4.5 mm/sec, section thickness of 3 mm, pitch of 1.5, 120 kVp, and either 240 or 220 mA. The scans were reconstructed in 2-mm section increments with a retrospectively targeted small (25-cm) field of view and a pixel size of 0.49 x 0.49 mm by using a standard reconstruction algorithm. Because we focused on imaging of the pancreas, the entire liver was not evaluated in the early and portal venous phases. For precontrast and delayed phase imaging of both the liver and pancreas, a craniocaudal scanning direction with a beam collimation of 7 mm was used in the nonhelical mode.
MR imaging protocol.—All imaging was performed with a 1.5-T superconducting magnet (Magnetom Vision; Siemens Medical Systems, Erlangen, Germany) by using a standard phased-array coil (Siemens Medical Systems) with four elements. After axial, fat-saturated T1-weighted fast low-angle shot (FLASH) (repetition time msec/echo time msec, 150/4.1) and respiratory-triggered turbo spin-echo (3,000–5,000/90) sequences were performed, dynamic MR images with gadopentetate dimeglumine (Magnevist; Schering) enhancement were obtained. Before and after rapid (2 mL/sec) manual injection of gadopentetate dimeglumine (0.1 mmol/kg), axial T1-weighted FLASH (150/6, 75° flip angle) MR images were obtained at 30, 60, 90, and 240 seconds in a breath hold. Arterial phase images were usually obtained at 30 seconds; portal venous phase images, at 90 seconds; and delayed phase images, at 240 seconds.
In some patients, the timing at 30 seconds was too early to obtain arterial phase images. In these cases, we used images obtained at 60 seconds as arterial phase images. A rectangular field of view of 213 (phase) x 340 (frequency) mm and a matrix of either 160 x 256 (matrix size, 2.04 x 1.03 mm) for fat-saturated FLASH and turbo spin-echo imaging or of 160 x 512 (size, 1.33 x 0.66 mm) for dynamic MR imaging were used. For the dynamic study, the frequency resolution was increased while limiting the phase-encoding steps to result in nonsquare pixels. A section thickness of 8 mm, intersection gap of 20%, and identical section locations were used in all acquisitions (subject to any inconsistencies in breath hold).
The imaging time was 18 seconds for the fat-saturated FLASH sequences and 19 seconds for the dynamic FLASH sequence. In the respiratory-triggered turbo spin-echo sequence, the acquisition time varied, depending on the repetition time; it ranged from 149 to 319 seconds (mean, 251 seconds) for 14 sections. The total examination time was approximately 30 minutes.
Image Analyses
CT and MR reading sessions were carried out separately and independently by two abdominal radiologists who have similar experience (more than 7 years) in both CT and MR imaging and had not seen these cases previously; the interval between the two readings was 3 weeks. For the CT and MR image readings, both arterial and portal venous phase images were simultaneously read, but combined readings of the two types of images were not performed for the ROC analysis. The readers did not know the surgical or histopathologic examination findings or the intraoperative US results, but the transabdominal US findings were made available at the time of the CT scan and MR image readings.
Initially, the two independent readers evaluated the image quality for the dynamic studies during the CT and MR examinations. Film hard-copy images in each examination were reviewed. The readers assessed the images for enhancement of the normal pancreas, vascular opacification, and presence of artifacts (chemical shift, susceptibility, and vascular ghosting artifacts on MR images and respiratory blurring on CT scans and MR images) by using a scoring system of 0 to 2, where 0 indicated a poorly enhanced pancreas, poorly depicted vessels, or severe artifacts; 1, a moderately enhanced pancreas, moderately depicted vessels, or slight artifacts; and 2, a well-enhanced pancreas, clearly depicted vessels, or the absence of artifacts. Discrepancies in scores were solved by using consensus. Nonparametric rank tests were used to compare scores in both imaging groups for every parameter, and a P value of .05 or less was considered to be statistically significant.
Second, local tumor extension was evaluated. Peripancreatic invasion was diagnosed when irregular signal intensity or soft-tissue streaks and strands in the peripancreatic fat layer were seen (1,11). Because a histopathologic examination could not be performed when the lesions were nonresectable, we could not tell whether the peripancreatic invasion was due to the tumor itself or to associated fibrosis. A vessel was considered to be nonresectable if it showed a focal reduction in caliber, circumferential encasement by the tumor, or frank thrombosis. We assumed that a vessel was involved with the tumor when more than half the circumference of the vessel was seen (7). No analysis of lymph nodes was performed.
To estimate the likelihood that a certain finding was present, the readers used a five-point confidence scale in which 5 indicated definitely present; 4, probably present; 3, indeterminate; 2, probably absent; and 1, finding not present. Each of the determinants of resectability—that is, tumor detection and invasion into the peripancreatic tissue, peripancreatic artery (celiac, hepatic, splenic, or superior mesenteric artery), and/or portal vein (main portal, splenic, or superior mesenteric vein)—was assessed.
To compare CT and MR imaging performance, we compared the ROC curves constructed for the two techniques. For each imaging method, a binominal ROC curve was fitted to each observer's confidence rating data by using a maximum likelihood estimation. The diagnostic accuracy of each imaging technique was determined by calculating the area under each reader-specific binominal ROC curve (Az). The differences between ROC curves for the individual readers were tested for significance by using the CORROC (statistical comparison of ROC curves estimated from correlated data sets) algorithm. The differences between the imaging techniques in terms of mean Az scores were analyzed statistically by using the Student two-tailed t test for paired data (18,19). The number of lesions correctly judged to be probably present (n = 4) or definitely present (n = 5) with ROC analysis by each reviewer was regarded as the number of correctly diagnosed lesions. The sensitivity, specificity, and accuracy of each sequence were evaluated.
For analysis of interobserver variability in the detection of lesions and evaluation of invasion with each imaging modality, 
statistics were used to measure the degree of agreement between the two observers. values greater than 0 were considered to be indicative of a positive correlation. Values of up to 0.40 were considered to be indicative of a positive but poor correlation; 0.41–0.75, a good correlation; and greater than 0.75, an excellent correlation.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Image Quality
The image quality results are shown in Table 1. The pancreatic enhancement on helical CT scans was subjectively given a mean grade of 1.2, and that on dynamic MR images was subjectively given a mean grade of 1.3; this difference was not statistically significant. Peripancreatic vessels were significantly more clearly depicted on helical CT scans (mean grade, 1.8) than on dynamic MR images (mean grade, 1.2). Image blurring was seen in two patients at helical CT; it was more frequently seen at dynamic MR imaging (in 10 patients). The susceptibility, chemical shift, and vascular ghosting artifacts seen on MR images occasionally caused difficulty in interpreting the images (in 15 patients).
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The results of analysis of lesion detection with CT and MR imaging are shown in Tables 2 and 3. Helical CT was slightly more accurate than was dynamic MR imaging in the detection of lesions (Table 2), and the area under the ROC curve was greater with helical CT (Table 3), but neither difference was significant. In lesions confined to the pancreas (in 11 patients), the tumor was somewhat more conspicuous on the MR images, but its detectability with MR imaging was similar to that with CT (Fig 1); eight tumors each were detected with CT and MR imaging. Neither CT nor MR imaging depicted three tumors less than 1.5 cm in diameter that were confined to the pancreas; however, these lesions were detected at endoscopic US or intraoperative palpation. A false-positive diagnosis of cancer was made in four (reviewer 1) and five (reviewer 2) patients at CT and in nine (reviewer 1) and eight (reviewer 2) patients at MR imaging. When the lesion extended beyond the pancreas (20 patients), detectability of the pancreatic tumor itself was greater on the CT scans (Fig 2). Nineteen such tumors were detected at CT compared with 14 detected at MR imaging by reviewer 1. Reviewer 2 detected 18 tumors that extended beyond the pancreas at CT compared with 14 detected at MR imaging.
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Resectability of Major Peripancreatic Vessels and Portal Veins
At surgery, 20 peripancreatic major arteries (nine common hepatic arteries, five superior mesenteric arteries, three celiac arteries, and three splenic arteries) in 18 patients were nonresectable, and 21 portal or superior mesenteric veins in 21 patients were nonresectable; these findings were confirmed by means of surgical palpation with US assistance. Among the nonresectable arteries, 15 were detected with CT and nine were detected with MR imaging by reviewer 1; 16 nonresectable arteries were detected with CT and seven were detected with MR imaging by reviewer 2. Among the nonresectable portal venous systems, 19 veins were detected with CT and six were detected with MR imaging by reviewer 1; 17 nonresectable veins were detected with CT and eight were detected with MR imaging by reviewer 2. The results of ROC analysis revealed that CT was significantly more accurate than MR imaging (Fig 3) (P < .01) in the detection of both arterial invasion and portal venous invasion.
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= 0.92). The values for the detection of peripancreatic extension (0.74) and invasion into the portal vein (0.72) or peripancreatic artery (0.65) indicated good agreement. These values with MR imaging indicated excellent agreement for tumor detection (0.92) and good agreement for the detection of peripancreatic invasion (0.71), portal venous invasion (0.60), and peripancreatic arterial involvement (0.51). |
DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Helical CT has been used successfully in imaging of the pancreas because it provides excellent depiction of the details of pancreatic tissue and small vessels and a high level of parenchymal enhancement without respiratory misregistration (3,7,20–24). Because data are acquired from a volume of tissue in helical CT rather than section by section, this modality is suitable for the evaluation of small cancers, which theoretically could be overlooked on nonhelical CT scans, even with 5-mm section widths, because of respiratory misregistration. A high degree of vascular and tumor opacification was achieved by using helical CT compared with the previously routinely used dynamic CT examination (3,21). In this study, we obtained thin-section images of the pancreas by means of retrospective targeting with a narrow (3-mm) collimation protocol. In our phantom study (9), increased resolution with acceptable reduction in the signal-to-noise ratio was achieved by using this technique. The thin-section technique also enables better evaluation of vascular involvement by the tumor (25).
In the past, MR imaging had a limited role in the detection and staging of pancreatic cancers because of phase-shift artifacts and limited spatial resolution. The fat suppression technique reduces phase-shift artifacts, increases the dynamic ranges of the signal intensities of abdominal organs, and depicts the pancreas with higher signal intensity relative to that of the surrounding tissue (10,12,26). With recent advances in MR pulse sequences, small pixel size, gradient-echo T1-weighted MR images can be obtained in a breath hold. Anatomic details are now more clearly depicted, and lesions become conspicuous with reduced chemical shift and ringing artifacts. In addition, with the use of a phased-array coil, the signal-to-noise ratio remains within an acceptable range (11).
Because the pancreas is a vascular organ with an abundant arterial supply and rich network of capillaries, the characteristic parenchymal "blush" that appears during dynamic contrast-enhanced studies has enabled the depiction of tumors at CT or MR imaging. Investigating the differences in vascularity and background tissue between cancers by using nonspecific extracellular contrast material in CT or MR studies permits optimal tumor detection. With either CT or MR imaging, dynamic imaging after the administration of contrast material has proved to be useful in detecting and staging pancreatic cancer. In the early phase of the dynamic study, the pancreas shows markedly uniform enhancement; in the later phase, its signal intensity (at MR imaging) or attenuation (at CT) gradually diminishes. On the other hand, pancreatic cancers are usually desmoplastic and hypovascular and thus appear at MR imaging as low-signal-intensity areas or at CT as low-attenuating areas during the early phase.
There have been few studies, however, in which dynamic helical CT was compared with dynamic MR imaging (10,12). Ichikawa et al (11) performed their dynamic MR study by using a 256 x 512 matrix and thin sections. Their MR imaging technique showed better performance than did helical CT in the identification of tumor, peripancreatic extension, and vascular involvement. However, in the present study, we found significantly better performance in the detection of peripancreatic tissue invasion and peripancreatic vascular invasion with helical CT, but the tumors were somewhat more conspicuous on the dynamic MR images. The difference between the results of the study by Ichikawa et al and those of this study may be due to the difference in CT technique. Ichikawa et al used 5-mm collimation with a standard field of view, whereas we used 3-mm collimation with a small field of view. The difference in spatial resolution between these two collimation techniques is substantial.
Theoretically, dynamic MR imaging has several potential advantages over dynamic CT. MR imaging has better contrast enhancement sensitivity and temporal resolution for whole-organ coverage and allows the administration of a more compact bolus for the contrast material injection. Breath-hold MR imaging provides better image quality than does the non–breath-hold technique. However, because imaging must be completed within a breath-hold period, the spatial resolution at MR imaging is substantially lower than that at CT owing to limited phase-encoding steps. The spatial resolution at CT can be increased by using the targeted thin-section technique. Furthermore, a breath hold of at least 16 seconds is required in multisection dynamic MR imaging, and this occasionally causes image blurring. In our study, there were several patients who could not hold their breath for 16 seconds and thus started to breathe. With helical CT, even if the patient cannot tolerate breath holding at the end of scanning, the quality of the majority of the sections will not be degraded by the resultant artifact. In our study, chemical shift, susceptibility, and vascular ghosting artifacts were unavoidable with MR imaging and caused difficulty in interpreting the fine details of peripancreatic and vascular invasion.
We found the three-dimensional data acquisition in helical CT to be useful in assessing vascular invasion. Although definite criteria for vascular invasion have not been established, thin-section helical CT after the intravenous administration of a bolus of contrast material reportedly increases the ability to assess vascular involvement by pancreatic cancer (25,27). In our study, at MR imaging, including dynamic studies, data were acquired with the two-dimensional multisection technique. Evaluation of vascular invasion was extremely difficult owing to the large section thickness and intersection gaps. Three-dimensional gradient-echo sequences have been used for vascular imaging. However, these sequences are mainly designed for imaging the vessels. We used this technique several times, but the signal-to-noise ratio and soft-tissue contrast were poor because of the extremely short repetition time. In the future, a fast three-dimensional data acquisition technique optimized for nonvascular imaging may help resolve the potential drawbacks of two-dimensional MR imaging.
Although diagnostic capability has substantially improved with recent developments in CT and MR imaging techniques, it is often difficult to detect very small tumors confined to the pancreas. Neither CT nor MR imaging demonstrated three tumors smaller than 1.5 cm in diameter that were confined to the pancreas. These tumors were detected only by using endoscopic US or at intraoperative palpation. The false-positive diagnosis of cancer of the pancreas in patients with chronic pancreatitis remains a diagnostic dilemma (14). Unless ancillary features of chronic pancreatitis are evident, differentiating these two entities may be impossible with the current techniques.
By taking advantage of the fine spatial resolution and consistency provided by the current CT technology, one can successfully use CT in tumor detection and staging. The sensitivity and accuracy of MR imaging seem to be inferior to those of CT owing to the limited spatial resolution and various artifacts, including chemical shift, motion, pulsation, and susceptibility artifacts, associated with MR imaging. The circumstances in which MR imaging may be useful include those in which (a) the clinical and CT findings are discordant, (b) the CT findings are indeterminate (16), or (c) the patient is allergic to iodinated contrast material.
A major disadvantage of the CT imaging protocol in this study is that the liver could not be fully evaluated by using our scanning parameters. We performed liver imaging before contrast material administration and during the delayed phase. Ideally, a CT protocol in which staging of pancreatic carcinoma is attempted should involve scanning of the liver to assess for the presence of hepatic metastases. However, the importance of the portal venous phase in imaging pancreatic carcinoma has been reported (8,28). Therefore, we chose to reduce the collimation in the early and portal venous phases to 3 mm and used a narrow field of view to increase the spatial resolution. Multisection helical scanners will make it possible to perform both portal venous phase hepatic imaging and thin-section pancreatic imaging.
The second limitation of our study is that histopathologic confirmation of all the imaging findings could not be obtained because 11 of the 31 tumors were nonresectable; however, a diagnosis of the tissue was made in all patients. Manual palpation of a pancreatic mass fixed to retropancreatic vessels indicates tumor resectability. In this study, although vascular involvement was confirmed at surgical palpation, the results of histologic examination confirmed the absence of invasion. Abundant fibrosis and many inflammatory changes surrounded the vessels. Further histopathologic comparison with helical CT or dynamic MR imaging findings would be necessary to establish the criteria for tumor invasion. Third, we did not evaluate lymph node swelling. This is because most of the metastatic tumors were small, and sometimes they were microscopic. This may have created a bias toward better results with both CT and MR imaging.
In conclusion, our study results demonstrated that, compared with MR imaging, thin-section helical CT may have more useful applications in the diagnostic imaging of pancreatic tumor. Thin-section helical CT of the pancreas enables detection of the tumor and evaluation of invasion into the peripancreatic tissue, peripancreatic artery, and/or portal vein.
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, Y.Y.; study concepts and design, Y.Y.; definition of intellectual content, T.T., M.T.; literature research, T.N.; clinical studies, T.N.; data acquisition, K.M.; data analysis, Y.N., Y.A.; statistical analysis, Y.A.; manuscript preparation, Y.Y.; manuscript editing, T.N.; manuscript review, M.T.
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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