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1 Department of Radiology, University "Federico II," Via Pansini 5,
80131 Napoli, Italy.
2 National Research Council, Via Pansini 5, 80131 Napoli, Italy.
3 Department of Radiology, New York University School of Medicine, 550 First
Ave., New York, NY 10016.
Received July 12, 2001;
accepted after revision December 6, 2001.
Address correspondence to M. Imbriaco, Via Manzoni 214/0, Parco Flory,
Isolato 4, Apt. 1, 80123, Napoli, Italy.
Abstract
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SUBJECTS AND METHODS. We studied 60 patients (31 men, 29 women; age range, 31-84 years; mean age, 62 years) with suspected pancreatic malignancy. Patients were randomly assigned to one of two groups. For group A (n = 30), unenhanced scans through the liver and pancreas were followed by two separate acquisitions (dual-phase) at 20-25 and at 60-80 sec after IV contrast administration. For group B (n = 30), unenhanced scans were followed by one set of scans (single-phase) acquired caudocranially (from the inferior hepatic margin to the diaphragm) starting 50 sec after IV contrast administration. Two observers independently scored images for the presence of tumor and for assessment of tumor resectability.
RESULTS. Comparison of dual-phase versus single-phase helical CT for
tumor detection showed a diagnostic accuracy for observer 1 of 87% and 90%,
respectively, and for observer 2, of 90% and 87%, respectively. For both
helical CT techniques, the overall agreement between the two observers was 83%
(
= 0.73 ± 0.03) for single-phase helical CT and 90% ( =
0.89 ± 0.03) for dual-phase helical CT. The assessment of resectability
was affected by the low number of resectable tumors (n = 8).
CONCLUSION. Single-phase helical CT is effective for the diagnosis and assessment of resectability of patients with suspected pancreatic carcinoma. Advantages are the lower radiation dose and fewer images to film and store.
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Single-detector helical CT is established as a highly accurate imaging technique for the diagnosis and staging of pancreatic ductal adenocarcinoma. Imaging protocols take advantage of the speed of acquisition and the ability to obtain thin sections to optimize differentiation among the tumor, normal pancreatic tissue, and surrounding blood vessels. However, controversy still exists about the optimal time window in which to image the pancreas. Graf et al. [4] have shown that arterial phase scanning of the pancreas is inferior to portal phase scanning for evaluating pancreatic carcinoma. Conversely, Tabuchi et al. [5] showed that early-phase helical CT is better than late-phase CT in revealing tumors, tumor size, and retroperitoneal invasion. In agreement with this latter study, several authors have shown the superiority of an early phase of acquisition with regard to tumor detectability compared with a late-phase helical CT acquisition [3, 6]. Lu et al. [7] have shown that the best timing for pancreatic imaging is in what they call the "pancreatic phase," the time between the conventional arterial and portal vein phases.
This prospective study was undertaken to compare dual-phase and single-phase helical CT in the detection and assessment of resectability in patients with suspected pancreatic cancer. In particular, we propose a helical CT technique for evaluating patients with pancreatic carcinoma that allows study of the pancreas in one single phase of acquisition in the reverse direction of traditional scanning protocols. Although this approach was first proposed by Megibow [8] in 1992 using a dynamic bolus-enhanced incremental scanning CT technique, to the best of our knowledge this technique has never been evaluated using helical CT.
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The preoperative criteria for definitely nonresectable cancer included the presence of distant metastases in the liver or peritoneal cavity, direct extension into surrounding organs or adjacent tissue, involvement of the neighboring major arteries and veins (i.e., superior mesenteric vein and artery and celiac axis), and lymphadenopathy greater than 1.5 cm. If the tumor was found to be nonresectable at laparotomy, surgical biopsy and bypass surgery (i.e., gastrojejunostomy combined with biliary jejunostomy) were performed.
CT Techniques
CT scans were obtained using a helical CT scanner (A-TOM XR LIBRA; Hitachi,
Tokyo, Japan). Thirty minutes before the examination, patients were given 500
mL of an iodinated oral contrast agent (Prontobarium-CT [barium sulfate];
Bracco, Milan, Italy) for the demarcation of the stomach and duodenum from the
adjacent organs. An 18-gauge catheter was placed in an antecubital vein.
Glucagon was not administered. Nonionic contrast material (150 mL) (Iopamiro
[iopamidol]; Bracco, Milan, Italy) with an iodine content of 300 mg I/mL,
injected using a power injector at a rate of 4 mL/sec, was administered to
both groups of patients. For dual-phase helical CT (group A), unenhanced scans
were followed first by an arterial phase scan 20-25 sec after the start of IV
contrast administration in the craniocaudal direction and next by a portal
phase scan at 60-80 sec after the start of IV contrast administration in the
reverse caudocranial direction. For single-phase helical CT (group B),
unenhanced scans were followed by one set of scans in the caudocranial
direction from the inferior hepatic margin to the diaphragm with a scanning
delay of 50 sec after the start of IV contrast administration. For both
protocols, scanning was performed with a breath-hold technique in 1 sec per
gantry rotation with a table speed of 5 mm/sec, a beam collimation of 5 mm,
3-mm reconstruction intervals, 120 kVp, a 35-cm field of view, and either 240
or 220 mA.
CT Image Interpretation
CT scans were interpreted from film separately and in a random order by two
gastrointestinal radiologists. The observers worked independently and at the
time of interpretation were unaware of findings from other imaging tests,
patients' clinical histories, and surgical or histopathologic findings. The
results of the interpretation were recorded on forms produced especially for
the project. Three-dimensional reconstruction was not used to evaluate
resectability. For both phases of imaging, observers scored the presence or
absence of tumor using a 3-point confidence scale (1 = no tumor; 2 =
indeterminate; and 3 = definite tumor). Interpretations scored as
indeterminate were considered positive in the specificity and sensitivity
calculations and therefore were attributed to definite categories.
In addition, for assessment of tumor resectability, observers scored the presence of resectable or nonresectable tumor using the following scores: 1, resectable; 2, indeterminate; and 3, nonresectable. The observers were told that lesions should be classified as nonresectable if evidence existed of peripancreatic vascular invasion (defined as encasement of the celiac, hepatic, or superior mesenteric artery or the portal or superior mesenteric vein). A vessel was considered involved if it showed a focal reduction in caliber, circumferential (>180°) encasement by tumor, or frank thrombosis. Involvement of the splenic artery or veins was not considered an absolute contraindication for resection unless the tumor extended into the splenoportal confluence or involved other splanchnic vessels.
Other criteria for nonresectability were extrapancreatic invasion of adjacent tissues and organs other than the duodenum, the presence of hematogenous or distant lymph node metastases (other than peripancreatic nodes), or signs of peritoneal carcinomatosis. A tumor was considered nonresectable if the diameter of a distant lymph node exceeded 1.5 cm. A tumor was defined as resectable if it was considered completely removable with surgery. The findings of the imaging modalities were then correlated with the final diagnosis.
After the administration of contrast material, mean CT attenuation values (in Hounsfield units) of normal pancreatic parenchyma, the liver, and the pancreatic tumor were obtained for both imaging protocols by means of regions of interest analysis. These measurements were made in the normal pancreatic parenchyma using 1-cm-diameter regions of interest in a region adjacent to the tumor rather than in an area remote from the tumor site, where normal parenchyma enhancement may vary slightly. Attenuation values for the pancreatic tumor were obtained in hypodense portions of the tumor; cystic areas were avoided Using the dual-phase protocol, attenuation was measured at the same slice locations in the normal pancreas, the liver, and the pancreatic tumor of CT scans obtained during the arterial and portal phases of acquisition to ensure direct quantitative analysis between the two phases.
For the quantitative analysis, we considered only patients with tumors (n = 35) and did not include patients with chronic pancreatitis, because the goal of this study was to compare dual-phase and single-phase CT for the detection of pancreatic cancer.
Vascular opacification of the celiac axis, the superior mesenteric artery, the superior mesenteric vein, and the portal and splenic veins was qualitatively assessed. Observers graded vascular opacification using a 3-point confidence scale (1 = not opacified; 2 = well opacified; and 3 = brightly opacified).
Statistical Analysis
The findings of imaging studies were classified as true-positive,
true-negative, false-positive, or false-negative for malignancy on the basis
of histopathologic results. Sensitivity, specificity, and diagnostic accuracy
were determined using standard criteria
[9]. For analysis of
interobserver variability in the detection of tumor and assessment of
resectability, Cohen's kappa statistic was used to measure the degree of
agreement between the two observers for single-phase helical CT. Kappa values
greater than 0 were considered to be indicative of a positive correlation.
Comparison between diagnostic capability of dual-phase and single-phase
helical CT was performed using the McNemar test.
Pancreatic parenchyma, liver, and pancreatic tumor attenuation values for both imaging protocols were compared using a paired two-tailed Student's t test. Vascular opacification was compared using Wilcoxon's signed rank test. Values for p of less than 0.05 were considered statistically significant.
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= 0.73 ± 0.03); dual-phase helical CT showed an overall agreement for
tumor detection between the two observers of 90% (27/30; = 0.89
± 0.03).
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Table 4 shows the quantitative measurements of enhancement of normal pancreatic parenchyma, liver, and pancreatic tumor in both the arterial and portal vein phases for dual-phase (group A) and for single-phase (group B) techniques in the 35 patients with pancreatic tumors. Using the dual-phase technique, enhancement of the pancreatic parenchyma was significantly greater during the portal vein phase than in the arterial phase (p < 0.0001). The degree of enhancement of pancreatic parenchyma using the single sequence was not significantly different from the levels of enhancement we achieved using the standard dual-phase technique. Furthermore, the degree of liver enhancement was significantly greater during the portal vein phase of the dual-phase technique and during the single-phase protocol than during the arterial phase (p < 0.0001). The degree of enhancement of solid tumor using the standard dual-phase technique was not statistically significant different from the degree of enhancement using the single-phase protocol. Finally, the mean difference between tumors and normal pancreatic parenchyma was slightly better for the single-phase technique (64 ± 10 H) than for the portal dual-phase technique (62 ± 27 H); however, this difference was not statistically significant.
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Using the dual-phase technique, a significantly greater degree of arterial opacification was present on arterial phase images, whereas a significantly greater degree of venous opacification was present on venous phase images (p < 0.0001). Using the single-phase technique, no statistically significant differences were observed between arterial and venous opacification. Figures 1A,1B,1C and 2A,2B show examples of nonresectable and resectable (respectively) pancreatic cancer detected using the single-phase helical CT technique. Figure 3A,3B shows an example of a nonresectable tumor of the pancreatic head detected using the dual-phase helical CT technique.
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Another report suggested a different approach for dual-phase helical CT in patients with pancreatic cancer [7]. Using a narrow collimation and a 40-sec scanning delay for the first helical sequence, Lu et al. [7] suggested that the pancreas is optimally scanned in a time window they call the pancreatic phase. During this phase, tumor—pancreas contrast is maximal, with adequate portal vein and arterial opacification. Subsequently, in a second helical CT sequence with a wider collimation and a scanning delay of 70 sec, the liver is scanned in a time window the authors call the hepatic phase. This second phase of image acquisition is performed during peak hepatic enhancement and is designed to optimize the detection of hepatic lesions [17, 18].
In a more recent study, Boland et al. [19], using dynamic thin-section helical CT, showed that contrast attenuation differences between pancreatic carcinoma and normal parenchyma are best shown with pancreatic phase helical CT. In agreement with this latter study, McNulty et al. [20] recently showed that a combination of pancreatic parenchymal phase and portal vein phase imaging is sufficient for the detection of pancreatic adenocarcinoma because that combination provides maximal pancreatic parenchymal and peripancreatic vascular enhancement. In particular, those authors, using a multidetector CT technique, observed greater pancreatic parenchyma enhancement during the pancreatic parenchymal phase (scanning delay, 35 sec) than during the portal vein phase (scanning delay, 60 sec). However, the tumor-to-parenchyma attenuation differences during the pancreatic parenchymal phase and the portal vein phase were similar. The differences between these latter results and previous studies [7, 19] using single-detector helical CT can be explained by the greater anatomic coverage achieved in a shorter scanning time when using multidetector CT [20].
In 1992, Megibow [8] was the first to propose a reverse direction of traditional scanning protocols using a dynamic incremental bolus CT technique for imaging patients with suspected pancreatic carcinoma. In that study, the first section was acquired at the level of the transverse duodenum (superior margin of L3), and subsequent sections were acquired as the patient moved in a caudocephalad direction. This protocol ensured that data acquisition occurred when the major arteries (celiac, hepatic, splenic, superior mesenteric, gastroduodenal, and pancreaticoduodenal) and veins (portal, splenic, and mesenteric) were intensely opacified. Furthermore, the pancreas itself was intensely enhanced.
We have described a CT approach for imaging of pancreatic cancer using a single-phase of acquisition in a caudocranial fashion, starting from the inferior hepatic margin of the diaphragm with a scanning delay of 50 sec from the beginning of IV contrast administration. To the best of our knowledge, this protocol using a helical CT technique has never before been proposed. The technique used in our study offers several advantages over conventional dual-phase helical CT. The imaging protocol is less complicated and less time-consuming for the technologist in terms of both image acquisition and recording on film. Film costs, demands on equipment, and radiation dose to the patients are also reduced. In addition, our protocol allows good opacification of both peripancreatic venous and arterial structures. Finally, another important advantage of our protocol is that the liver and the entire upper abdomen can be fully evaluated during the portal phase, which is known to be the best temporal window for identification of liver metastases and other ancillary tumor findings (such as ascites in patients with pancreatic cancer).
As can be seen from the quantitative data, the degree of enhancement in Hounsfield units of the normal pancreatic parenchyma using the single sequence is not statistically significantly different from the levels of enhancement we achieved using the standard dual-phase technique. In addition, the mean difference between tumor and normal pancreatic parenchyma, although not statistically significant, was slightly better for the single-phase than for the dual-phase technique.
These findings provide an additional argument that a single-phase protocol can compete with the dual-phase technique for the detection of tumors in patients suspected of having pancreatic carcinoma. Furthermore, the hepatic parenchyma was enhanced at a time close to the peak hepatic enhancement, which optimizes the detection of hepatic lesions. Finally, using the single sequence, no statistically significant differences were observed in the degree of opacification of either peripancreatic arteries or veins. Evaluation of the status of these vessels is of major importance in determining resectability of tumors in the pancreatic head and neck. At our institution, surgeons will not attempt resection of a pancreatic neoplasm if major venous involvement is documented; we consider such a tumor nonresectable. This practice is not universal; aggressive surgical approaches at some institutions will incorporate mesenteric venous resection and repair if necessary [21]. In these cases, accurate CT visualization of the presence of venous involvement is useful for the surgeon.
As previously shown by Megibow [8], potential problems exist with the reverse-direction technique. Variants in pancreatic morphology or scoliosis will occasionally result in the inferior margin of the gland being below the level of L3. In addition, the patient may have a Riedel's lobe of the liver, and the tip of the right lobe will not be included. To overcome these problems, we prefer to start our acquisition from the bottom of the liver and continue through the entire diaphragm. In our series, no patient was excluded from the study because of lack of inclusion of the entire pancreas or liver on the scan.
Another potential limitation of our study is that we did not attempt to compensate for physiologic differences in patients by means of a test dose technique or by using a semi-automated scanning delay. We standardized all scans during the portal phase to begin 50 sec after the start of the contrast injection. Further studies are required to determine if the scanning delay can be customized using a technique such as SmartPrep (General Electric Medical Systems, Milwaukee, WI) to optimize pancreatic enhancement.
A single-phase helical CT acquisition performed with a scanning delay of 50 sec after the beginning of IV contrast administration may not be the ideal method for detecting hypervascular pancreatic tumors such as islet cell tumors. In these particular cases, with a high degree of clinical and laboratory suspicion, a dual-phase protocol with an early arterial phase (20-25 sec) acquisition should be preferred to the single-phase technique.
In conclusion, the results of our study show that for tumor detection and assessment of resectability in patients with pancreatic carcinoma, dual-phase and single-phase helical CT show comparable diagnostic accuracy. Although further studies—particularly with the faster multidetector CT scanners—are required to validate these findings, taking into account the greater anatomic coverage that can be achieved in a shorter time, a single-phase acquisition in a caudocranial direction might be suggested as the protocol of choice when evaluating patients with suspected pancreatic cancer using single-detector helical CT.
Acknowledgments
We sincerely thank Graciana Diez-Roux for critically reviewing this paper
and Carmela Imparato for editing the manuscript.
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