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1 Department of Radiology, Stanford University Medical Center, 300 Pasteur Dr.,
Room H1307, Stanford, CA 94305.
2 Present address:Department of Radiology, Southern Illinois University 1520 S
Second St., #1103, Springfield, IL 62701.
3 Department of Radiology, Veterans Administration Palo Alto Health Care System,
3801 Miranda Ave., Palo Alto, CA 94304.
4 Department of General Surgery, Stanford University Medical Center, Stanford,
CA 94305.
Received July 5, 2003;
accepted after revision September 3, 2003.
Address correspondence to R. B. Jeffrey, Jr.
(bjeffrey{at}stanford.edu).
Abstract
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MATERIALS AND METHODS. Imaging findings related to vascular invasion and overall tumor resectability in 25 patients who underwent contrast-enhanced biphasic MDCT evaluation were correlated with actual vessel invasion and overall resectability determined at surgery and pathologic examination. The presence of vascular invasion was assessed in 110 major peripancreatic vessels in 22 patients who underwent resection.
RESULTS. On MDCT, 23 (92%) of 25 patients were deemed to have resectable pancreatic adenocarcinoma. The tumors in the remaining two (8%) were considered not resectable because of the presence of vascular invasion (which was confirmed in only one patient at surgery). Of those 23 patients deemed to be candidates for curative resection on the basis of MDCT results, 20 were found to have resectable adenocarcinoma at time of surgery, yielding a negative predictive value for MDCT of 87% (20/23 patients) for overall resectability. In the other three patients, adenocarcinoma was deemed to be unresectable because of small metastases to the liver (two patients) or to the peritoneum (one patient) discovered at surgery. For detection of vascular invasion, MDCT yielded a negative predictive value of 100% (108/108 vessels) with no false-negative findings and an accuracy of 99% (109/110 vessels) with 108 true-negative findings, one true-positive finding, and one false-positive finding.
CONCLUSION. Our preliminary data on MDCT show that the technique has excellent negative predictive value for vascular invasion and good negative predictive value for overall tumor resectability in patients with pancreatic adenocarcinoma, suggesting an improvement over previous results reported using single-detector CT. The problem of undetected micrometastases to the liver and peritoneum remains.
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Recently, the introduction of MDCT has offered a substantial improvement in volume coverage speed with no loss of image quality [6], facilitating optimal pancreatic parenchymal and peripancreatic vascular enhancement [7]. In addition, MDCT facilitates the generation of multiplanar reconstructions, such as curved planar reformations, providing the potential to improve the detection and staging of pancreatic adenocarcinoma [8–10]. The purpose of our study was to determine the negative predictive value of MDCT with curved planar reformations for detecting vascular invasion and predicting overall tumor resectability in patients with pancreatic adenocarcinoma.
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Through the review of the aforementioned radiologic, surgical, pathologic, and clinical reports, we identified 59 patients (18%) with newly diagnosed pancreatic adenocarcinoma. According to the surgical reports, only 27 of these patients underwent surgery for a potentially curative resection. In the 32 patients who did not undergo surgery, a final diagnosis of pancreatic adenocarcinoma was confirmed with biopsy in 23 patients and with clinical studies (medical history, laboratory data, and imaging findings) in nine patients. In none of these 32 nonsurgical patients was resectability or absence of vascular invasion predicted from the MDCT findings.
Our interest was the group of 27 patients for whom surgical and pathologic findings were available for correlation with MDCT findings. Two of these patients were excluded, however, because they had received a course of external beam radiation therapy before surgery. Thus, our study group comprised 25 patients—12 women and 13 men with a mean age of 64.3 years (range, 43–79 years)— with pancreatic adenocarcinoma who underwent surgery for possible tumor resection after assessment on MDCT. The primary author, a fourth-year medical student, and a radiologist with expertise in abdominal imaging jointly reviewed the MDCT, surgical, and pathologic reports of the patients. The MDCT results (based on the prospective interpretations of the MDCT examinations) were correlated with the surgical and pathologic results. The mean interval between the MDCT evaluation and surgery was 13 days (range, 1–51 days). The institutional review board of our hospital approved this study.
Scanning Parameters
CT scans were obtained with an eight-detector CT scanner (LightSpeed QX/i;
General Electric Medical Systems, Milwaukee, WI) using a dualphase pancreatic
protocol. Initially, unenhanced scans were obtained using a 10- to 12-sec
breath-hold acquisition, 10-mm collimation, and a pitch of 6 (high-speed mode)
to define the target volume extending from the celiac axis to the transverse
duodenum to be subsequently scanned during the IV injection of contrast
material. Immediately before scanning, the patient was asked to drink 32 oz of
water as a nonopaque intraluminal contrast agent. After insertion of an 18- or
20-gauge catheter into an antecubital vein, 150 mL of iohexol 300 mg I/mL
(Omnipaque, Nycomed, Princeton, NJ) was injected at a rate of 4 mL/sec with a
power injector (Envision CT, Medrad, Indianola, PA). Forty seconds after
initiation of the injection, 1.25-mm nominal thickness sections were obtained
during a 15–20 sec breath-hold through the target volume using a pitch
of 6 (pancreatic phase). The images obtained during this phase were
reconstructed at 0.5-mm intervals using a 20-cm field of view. A second
breath-hold acquisition (portal venous phase) covering the area from the
diaphragm to the symphysis pubis was obtained 70 sec after initiation of the
injection of contrast material using 5-mm nominal thickness sections and a
pitch of 6. The images obtained during this phase were reconstructed at 5-mm
intervals using a large field of view. These data were then transferred to an
independent workstation.
Curved Planar Reformations
Curved planar reformations were generated using either an Advantage Windows
3.1 (General Electric Medical Systems) or a Vitrea 2.2 (Vital Images,
Minneapolis, MN) workstation. Images were obtained by placing a cursor on a
stack of axial, sagittal, coronal, or oblique sections along the course of the
specific anatomic structure. The plane thus delineated resulted in a 2D image
of average density that displayed the entire course of the anatomic structure
throughout the data set (Fig.
1A,
1B,
1C,
1D).
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The thickness of the curved plane is the voxel dimension perpendicular to the curved plane and depends on the orientation of the section on which it is drawn. The section thickness of the curved plane is never larger than the effective section thickness or smaller than the transverse pixel dimensions. Curved planar reformations are highly dependent on the accuracy of curve placement, may create artifactual lesions, or may not display eccentric lesions. Therefore, two orthogonal curved planes must be created through each structure including a curved transverse, curved sagittal, or curved coronal reformation.
Dedicated CT technologists in our 3D laboratory who have undergone physician-directed training in delineating vascular and bile and pancreatic ductal anatomy produced the curved planar reformations. Curved planar reformations were obtained to display the course of the pancreatic duct, common bile duct, celiac artery, hepatic artery, splenic artery, superior mesenteric artery, portal vein, superior mesenteric vein, and splenic vein (Fig. 2A, 2B, 2C, 2D).
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Correlation of Imaging Findings with Surgical and Pathologic Findings
MDCT reports at our institution routinely include a synthesis of the
interpretations of both the transverse scans and curved planar reformations.
We reviewed these reports for the following information: the size, location,
and attenuation of tumor; the degree of vascular involvement by tumor; and the
presence or absence of local extension by tumor or distant metastasis. At our
institution, pancreatic adenocarcinoma is commonly considered to be
unresectable if any of the following imaging findings is present:
extrapancreatic invasion of adjacent tissues or organs other than duodenum;
peritoneal carcinomatosis or distant metastases; or vascular invasion (defined
as tumor-to-vessel contiguity > 50%) of a major peripancreatic
vessel—the celiac artery, hepatic artery, portal vein, superior
mesenteric artery, or superior mesenteric vein. The superior mesenteric vein
is also considered unresectable if it reveals any degree of deformity;
however, some surgeons do not consider superior mesenteric vein invasion
necessarily to be an unresectable finding
[5,
11]. Imaging-based predictions
of vascular invasion and overall resectability were compared with findings of
actual vessel invasion and overall resectability found at surgery and with the
final pathologic results. Correlation between imaging findings and surgical
and pathologic findings of vascular involvement was determined on a
vessel-by-vessel basis.
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Twenty tumors (80%) were hypoattenuating, one (4%) was both hypo- and hyperattenuating, and four (16%) were considered isoattenuating relative to normal pancreatic parenchyma because no discrete mass was seen. In all four patients with isoattenuating tumors, dilatation of either the pancreatic or bile duct or both was visualized on MDCT. At surgery, three of the four isoattenuating tumors were found to be of the infiltrative type, involving the pancreatic head in one patient and the head and body of the pancreas in two patients. However, in the fourth patient, a 2-cm periampullary mass confirmed to be a pancreatic adenocarcinoma at pathology was not detected on MDCT. Thus, 21 of 22 tumors presenting as mass lesions were detected on MDCT, and in all three patients with infiltrative tumors, MDCT findings suggested that a tumor was present.
Twenty-two (88%) of 25 patients underwent tumor resection, and three (12%) were found to have unresectable disease at surgery because of either liver (n = 2) or peritoneal (n = 1) metastases. The sizes of liver metastases found at surgery were less than 1 cm in a patient in whom MDCT showed a normal liver and as large as 1.5 cm in a patient in whom MDCT showed clusters of small (< 1 cm) rim-enhancing areas of low attenuation in the liver that on MDCT were interpreted as small hepatic abscesses. In the patient with peritoneal metastases, multiple diffuse studding of the peritoneum from the diaphragm down to the pelvis was discovered at surgery. Among the 22 patients who underwent resection, one patient had an adenocarcinoma-positive vascular margin involving the superior mesenteric vein. The involvement was correctly identified preoperatively on MDCT as a 50% encasement and narrowing of the vessel (Fig. 3A, 3B). Another patient who underwent preoperative MDCT was described as having tumor that abutted and deformed the superior mesenteric vein, indicating probable adventitial invasion, but at surgery, no vascular invasion of the superior mesenteric vein was found (Fig. 4A, 4B, 4C).
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In summary, 21 patients underwent successful resection with negative tumor margins, one patient underwent resection with a positive vascular margin (as previously described), and three patients were found to be unresectable at time of surgery because of hepatic or peritoneal metastases that were not identified preoperatively on MDCT. Thus, in predicting overall tumor resectability, MDCT afforded a negative predictive value of 87% (20/23).
CT, surgical, and pathologic correlation was established for 110 major peripancreatic vessels in 22 patients who underwent surgical resection and inspection of vessels. On the basis of MDCT findings, 108 of 110 vessels were diagnosed as free of tumor invasion and two vessels (superior mesenteric vein in two patients) as invaded by tumor. At surgery, 109 vessels were identified as free of tumor and only one superior mesenteric vein was found to be invaded by tumor. Thus, for detecting vascular invasion by tumor on a vessel-by-vessel basis, MDCT yielded a negative predictive value of 100% (108/108) with no false-negative findings and an accuracy of 99% (109/110) with 108 true-negative findings, one true-positive finding, and one false-positive finding.
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CT is the imaging modality most frequently used for the evaluation of patients with suspected pancreatic adenocarcinoma. Maximal enhancement of the pancreatic parenchyma and peripancreatic vascular structures is important for the detection and staging of pancreatic neoplasms on CT. The recent development of MDCT allows the use of extremely thin collimation for the acquisition of high-resolution scans during multiple phases of contrast enhancement [9]. Thus, greater parenchymal, arterial, and portal venous enhancement may be achieved when imaging the pancreas with MDCT [7]. With these features, MDCT potentially offers an improvement in the early detection and accurate staging of pancreatic adenocarcinoma.
Previous studies using single-detector CT reported a sensitivity of more than 90% for detection of pancreatic adenocarcinoma and a positive predictive value in the range of 96–100% for determination of surgical unresectability [1–4]. However, single-detector CT is not as accurate for determining tumor resectability, with reported negative predictive values of 56% for uniphasic imaging [2] and 79% for biphasic imaging [3]. The most frequent reasons for tumor unresectability found at surgery are small (< 1 cm) liver metastases, lymph node metastases, vascular invasion, and small peritoneal metastases [2, 3]. Our results revealed a higher negative predictive value of 87% (20/23 patients). This value may not be statistically significant but indicates a trend towards improved prediction of resectability using MDCT compared with the predictive power using single-detector CT. Moreover, unlike previous studies, none of our three false-negative MDCT results was due to undetected vascular invasion; our false-negative results were due to small hepatic and peritoneal metastases not detected on preoperative MDCT in three patients.
Detection of small liver metastases and peritoneal implants remains one of the greater challenges in the preoperative staging of pancreatic adenocarcinoma [1–5]. Bluemke et al. [2] used single-phase single-detector helical CT to study 64 patients with pancreatic adenocarcinoma. Of the 19 patients with tumors that appeared resectable on CT but were found to be unresectable at surgery, eight (42%) had undetected liver metastases smaller than 10 mm in diameter, and one (5%) had undetected diffuse carcinomatosis. In a study of 76 patients by Diehl et al. [3] using biphasic single-detector helical CT, four (80%) of five patients incorrectly diagnosed as having resectable tumors were found to have small undetected liver metastases at surgery. Similarly, in our study, of the three cases in which pancreatic adenocarcinoma that appeared resectable on MDCT was found to be unresectable at surgery, two involved undetected small liver metastases; in the third unresectable case, undetected peritoneal implants were involved. The problem of undetected metastases, especially undetected hepatic metastases, has led many surgeons to routinely perform laparoscopy and laparoscopic biopsy before proceeding to radical pancreaticoduodenectomy [5].
In the absence of distant metastatic disease, vascular invasion is the single most common criterion for unresectability in patients with pancreatic adenocarcinoma [3]. Indeed, extraglandular extension of the tumor with invasion of adjacent arterial and venous structures is a common feature of advanced pancreatic adenocarcinoma. Detection of vascular invasion is key to the surgeon's preoperative planning because the posterior lateral surfaces of the portal vein and superior mesenteric vein can be evaluated only after the surgical procedure is well advanced and the duodenum and pancreatic neck are divided. In our study, correlation of MDCT findings with surgical and pathologic findings on a vessel-byvessel basis was established for five vessels considered critical by surgeons: the celiac artery, hepatic artery, superior mesenteric artery, superior mesenteric vein, and portal vein. To determine vascular invasion by MDCT appearance, we used criteria to assess the extent of contact between the tumor and the vessel similar to the criteria used by Lu et al. [11] and O'Malley et al. [16]: tumor involvement of any of the major peripancreatic vessels that exceeded one half of the circumference of the vessel indicated invasion and precluded a curative resection, and contour deformity of the superior mesenteric vein was considered a sign of invasion of this vessel. However, some surgeons do not consider superior mesenteric vein invasion necessarily to be an unresectable finding, as exemplified by our one true-positive case for vascular invasion in which the patient underwent resection despite this finding on preoperative MDCT.
The reported accuracy for determining vascular invasion using single-detector helical CT is in the range of 70–95% [3, 11, 16–18]. The studies by Lu et al. [11] of 25 patients and 80 vessels and by O'Malley et al. [16] of 25 patients and 98 vessels using single-detector helical CT yielded, respectively, an accuracy of 94% (one false-positive and four false-negative findings) and 92% (one false-positive and seven false-negative findings) for prediction of vascular invasion by tumor. Our study of 25 patients and 110 vessels yielded an accuracy of 99% and a negative predictive value of 100%, with no false-negative, one true-positive, and one false-positive result. Our results indicate a trend toward improved detection of vascular invasion with the use of MDCT.
The false-positive result for vascular invasion in our study involved a superior mesenteric vein. MDCT revealed that the tumor abutted and deformed the right lateral wall of the superior mesenteric vein, suggesting adventitial invasion; however, at surgery, the tumor was found to be resectable, and at pathology, the vein was confirmed to be uninvolved by the tumor. Similarly, the single false-positive result found in each of the studies by Lu et al. [11] and by O'Malley et al. [16] involved the superior mesenteric vein. Normally, the superior mesenteric vein may be directly contiguous to normal pancreatic parenchyma along its lateral and anterior margins. Therefore, a tumor involving this part of the pancreas can be contiguous to the vein without invading it. However, the tethered, teardrop appearance of the superior mesenteric vein described by Hough et al. [19], which presumably results from either direct tumor infiltration or peritumoral fibrosis adherent to the vessel, may be a reliable sign of tumor unresectability. Our false-positive result illustrates the difficulty that evaluation of invasion of the superior mesenteric vein still poses.
In three previous studies—Diehl et al. [3], Raptopoulos et al. [17], and Lepanto et al. [18]—multiplanar reformations were obtained in addition to standard transverse images, allowing comparison of the transverse and multiplanar imaging displays for accurate determination of vascular invasion. These authors reported varying results for determining vascular invasion of arteries versus veins. Diehl et al. [3] reported lower overall accuracy for multiplanar reformations than for transverse images (86% vs 92%). Furthermore, in that study, the accuracy for determining arterial invasion with multiplanar reformations was only 67%, whereas the accuracy for determining venous invasion with multiplanar reformations was 94%. Raptopoulos et al. [17] obtained higher accuracy for determining overall vascular invasion when transverse images were interpreted in combination with multiplanar reformations than when transverse images were interpreted alone (96% vs 70%). For determining arterial invasion with multiplanar reformations, Lepanto et al. [18] obtained accuracy values (86%) similar to those reported by Raptopoulos et al., but for determining venous invasion, they obtained higher accuracy values when transverse images were interpreted in combination with multiplanar reformations than when transverse images were interpreted alone (92% vs 69%).
Our study was based on the review of prospective interpretations of MDCT examinations, which at our institution routinely combine transverse images and curved planar reformations. It appears that based on the early experience with curved planar reformations reported by Prokesch et al. [9], transverse images are equivalent to curved planar reformations for use in determining vascular invasion. Other postprocessing imaging techniques used to evaluate the pancreas include minimum intensity projection, maximum intensity projection, and volume rendering. Minimum intensity projection is useful for displaying hypoattenuating structures such as the common bile duct and the pancreatic duct. Maximum intensity projection and volume rendering are useful for visualization of abdominal vascular structures [20]. At our institution, these techniques are used on a case-by-case basis.
A number of limitations in our study should be considered. First, the study was limited to the review of the radiologic, surgical, pathologic, and medical records. In addition, the number of patients included in the study group was small, and it is possible that the results would differ with a larger series. Our study focused on patients who had undergone surgery, so a selection bias toward potentially resectable tumors is introduced because only patients with such tumors tend to be referred for surgical evaluation. Finally, no surgical evaluation of vascular invasion was performed in the 32 nonsurgical patients with unresectable tumors; thus, it is possible that instances of false-positive findings of vascular invasion were unidentified.
In summary, the introduction of MDCT allows the use of extremely thin collimation and the acquisition of high-resolution images of the pancreas during greater parenchymal, arterial, and portal venous enhancement and potentially offers a more accurate staging of pancreatic adenocarcinoma. Our preliminary data with MDCT show that the technique has excellent negative predictive value for vascular invasion and good negative predictive value for overall tumor resectability in patients with this disease. Unfortunately, the problem of undetected micrometastases in the liver and peritoneum remains to be solved.
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