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1
Institut de Diagnòstic per la Imatge, Hospital Duran i Reynals, Ciutat
Sanitària i Universitària de Bellvitge, Autovia de Castelldefels
km 2, 7, L'Hospitalet de Llobregat, 08907 Barcelona, Spain.
2
Department of Surgery, Hospital Princeps d'Espanya Ciutat Sanitaria i
Universitaria de Bellvitge, C/Feixa Llarga s/n, L'Hospitalet de Llobregat,
08907 Barcelona, Spain.
3
Department of Pathology, Hospital Princeps d'Espanya, 08907 Barcelona,
Spain.
Received July 10, 2001;
accepted after revision October 18, 2001.
Address correspondence to C. Valls.
Abstract
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SUBJECTS AND METHODS. Between January 1999 and December 2000, 76
patients with suspected pancreatic cancer underwent preoperative evaluation
and staging with dual-phase helical CT (3-mm collimation for pancreatic phase,
5-mm collimation for portal phase). Iodinated contrast material was injected
IV (170 mL at a rate of 4 mL/sec); acquisition began at 40 sec during the
pancreatic phase and at 70 sec during the portal phase. Three radiologists
prospectively evaluated the imaging findings to determine the presence of
pancreatic tumor and signs of unresectability (liver metastasis, vascular
encasement, or regional lymph nodes metastasis). The degree of
tumor—vessel contiguity was recorded for each patient (no contiguity
with tumor, contiguity of <50%, or contiguity of 
50%).
RESULTS. Thirty-nine patients with pancreatic adenocarcinoma were surgically explored. Curative resections were attempted in 34 patients and were successful in 25. The positive predictive value for resectability was 73.5%. Nine patients considered resectable on the basis of CT findings were found to be unresectable at surgery because of liver metastasis (n = 5), vascular encasement (n = 2), or lymph node metastasis (n = 2). We found that the overall accuracy of helical CT as a tool for determining whether a pancreatic adenocarcinoma was resectable was 77% (30/39 patients).
CONCLUSION. Dual-phase helical CT is a useful technique for preoperative staging of pancreatic cancer. The main limitation of CT is that it may not reveal small hepatic metastases.
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The main role of preoperative staging procedures is to distinguish between potentially resectable and nonresectable patients so that unnecessary surgical procedures may be avoided; survival benefits can be achieved only in patients in whom the tumor can be completely resected. Because of recent improvements in radiologic techniques, a wide range of imaging tools is now available, such as helical CT, MR imaging, endoscopic sonography, endoscopic retrograde cholangiopancreatography, and angiography. However, at this point, no consensus exists as to the best staging algorithm. The aim of our study was to assess the results of helical CT used as the only procedure in the diagnosis and staging of pancreatic cancer in a large series of patients from a single institution. We sought to avoid invasive procedures such as endoscopic retrograde cholangiopancreatography. Our objective was to evaluate the results of helical CT in preoperative staging, focusing on either arterial or venous vascular invasion. We specifically assessed the relevance of small reticular opacities arising from the tumor and abutting an arterial vessel that we defined as "periarterial streaks."
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To be included in the study, patients had to have painless obstructive jaundice with sonographic evidence of intra- and extrahepatic bile duct dilatation or sonographically based suspicion of pancreatic mass. In our institution, the imaging algorithm of painless obstructive jaundice begins with sonography. If the sonographic examination discloses intra- and extrahepatic bile duct dilatation, we proceed directly to dual-phase pancreatic helical CT. If the dilatation involves only the intrahepatic biliary tree (with a normal extrahepatic bile duct), we perform dual-phase helical CT of the liver and MR cholangiopancreatography. For our study, we specifically refrained from using endoscopic retrograde cholangiopancreatography or biliary drainage before CT to avoid artifacts in the diagnostic study and complications related to infections.
Twenty-one patients were not considered candidates for surgical exploration because of poor clinical condition (n = 2) or advanced metastatic disease at CT (n = 19). Fine-needle aspiration biopsy was performed in all patients who did not undergo surgical exploration. Biopsy was not performed in candidates for surgical exploration. Eventually, 55 patients underwent surgical exploration within 1 week of their CT examination.
For analysis of preoperative staging, only patients with proven pancreatic adenocarcinoma who underwent surgical exploration were considered. Patients with periampular adenocarcinoma, islet cell cancer, distal bile duct cholangiocarcinoma, or other pancreatic conditions were excluded. Therefore, our final study group consisted of 39 patients with pancreatic adenocarcinoma who underwent surgical exploration. There were 24 men and 15 women with a mean age of 61.1 years (range, 38-78 years).
Helical CT Technique
Helical CT was performed with a ProSpeed Plus system (General Electric
Medical Systems, Yokogawa, Japan). Unenhanced images were obtained first to
locate the upper and lower limits of the pancreas so that the entire gland
would be included in the contrast-enhanced study. Either ionic (370 mg I/mL)
or nonionic (320 mg I/mL) iodinated contrast material (170 mL) was injected at
a rate of 4 mL/sec using a power injector (MCT; Medrad, Pittsburgh, PA).
Acquisition began at 40 sec for the pancreatic phase and 70 sec for the portal
phase. In the first helical acquisition, images of the pancreas were obtained
with a 3-mm collimation and a 5-mm interval from the lower to the upper levels
of the pancreas. Images were reconstructed at 3-mm intervals. In the second
helical acquisition, images of the liver and pancreas were acquired from the
dome of the liver to the lower level of the pancreatic gland with a 5-mm
collimation and a 7.5-mm interval. Images were reconstructed at a 5-mm
interval. Because of tube-heating limitations, we used 250-300 mAs and 120 kV
for thin-section pancreatic images and 250 mAs for the rest of the study. In
patients with suspected hemangiomas or liver cysts observed during the portal
phase imaging, delayed scans were also obtained.
Before the patients underwent surgical exploration, the CT images were prospectively assessed by at least two of three experienced abdominal radiologists in consensus. The pancreatic and portal phase images were interpreted at the same time. The imaging findings and preoperative CT diagnosis were recorded in an electronic database.
Preoperative Staging
For the staging procedure, we specifically evaluated signs suggesting or
indicating unresectable disease, such as vascular invasion and distant
metastasis.
Vascular invasion.—The degree of tumor-to-vessel
circumferential contiguity was recorded for each patient (no contiguity with
tumor, contiguity of <50%, or contiguity of 50%) for the following
vessels: celiac trunk, hepatic artery, superior mesenteric artery, superior
mesenteric vein, and portal vein. Tumor-to-vessel contiguity was defined as
direct tumor-to-vessel contact with complete obliteration of the fat plane.
Arterial invasion was defined as any direct tumor-to-vessel contiguity even if
the contiguity was less than 50% (Fig.
1). Small reticular opacities radiating from the tumor and
abutting an arterial vessel (so-called periarterial streaks) were not
considered arterial invasion. Venous invasion was defined as tumor-to-vessel
circumferential contiguity of 50% or more. Tumor-to-vein circumferential
contiguity of less than 50% was not considered venous invasion
(Fig. 2).
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Distant metastasis.—Liver metastases were defined as nodular low-attenuation lesions with diameters of more than 1 cm without characteristic findings of benign lesions, such as cysts or hemangiomas. Subcentimetric lesions were considered indeterminate and were not treated as metastases.
Enlarged lymph nodes (>1.5 cm) outside peripancreatic draining chains of the pancreas were considered metastatic. Substantial ascites and a large number of peritoneal nodules were considered evidence of peritoneal dissemination.
Criteria of unresectability.—A tumor was considered unresectable if one of the following features was found: distant metastasis either to the liver, regional lymph nodes, omentum, or adjacent organs except the duodenum; arterial invasion; any tumor-to-artery contiguity; or massive venous invasion, that is, tumor infiltration with thrombosis and obliteration of the vessel lumen. Venous invasion without thrombosis or obliteration of the lumen was not considered indicative of unresectable disease, and the surgeon was prepared for venous resection. All patients with questionable findings, such as periarterial streaks, were surgically explored.
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Surgical procedures were performed in 39 patients. In 34 patients, radical surgery was planned on the basis of preoperative imaging, whereas gastroenteroanastomosis and palliative surgery were planned in five patients with unresectable disease and duodenal invasion.
Curative resections were successful in 25 of 34 instances, a resectability rate of 73.5%. The positive predictive value of helical CT in regard to resectability was also 73.5% (25/34). Nine patients thought to have resectable disease on the basis of CT findings were found to have unresectable disease at surgery. In that subgroup of patients, the reasons for unresectability were liver metastases (n = 5), vascular encasement (n = 2), and lymph nodes metastases (n = 2). The overall accuracy of helical CT in revealing resectability or unresectability of pancreatic adenocarcinoma was 76.9% (30/39).
Liver Metastases
Liver metastases were found at surgical exploration in eight (20.5%) of 39
patients with pancreatic adenocarcinoma in whom surgery was performed. The
reason for unresectability in 55.5% (5/9) of patients believed to be
resectable on the basis of CT findings but found to be unresectable at surgery
was unsuspected liver metastasis. The average size of the lesions was 8 mm. In
two of these patients, retrospective evaluation of helical CT images disclosed
two tiny liver lesions. It is interesting that one of these lesions was
hypervascular in the pancreatic phase (Fig.
3A,3B).
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Lymph Node Metastases
Eighteen (52.9%) of 34 surgically explored patients had tumoral lymph node
involvement confirmed at surgery or pathologic examination. Helical CT
accurately identified metastatic lymph node involvement in 16.7% (3/18) of the
patients. These patients had lymph nodes larger than 1.5 cm and were
resectable because the metastatic lymph nodes affected peripancreatic nodes
and were resected en bloc with the primary tumor. In 39.8% (7/18) of the
patients with positive lymph nodes at histopathologic examination, helical CT
disclosed nonspecific lymph nodes with diameters of less than 1.5 cm. In the
remaining 44.4% (8/18) of these patients, helical CT did not reveal any lymph
node involvement.
Only 5.9% (2/34) of potentially resectable patients were found to be unresectable because of undetected lymph node metastasis. One of these patients had a left paraaortic lymph node of 1.7 cm that was missed prospectively. In the other case, lesions were not detectable in a retrospective evaluation.
Vascular Invasion
Superior mesenteric vein.—Superior mesenteric vein invasion
(tumor-to-vessel contiguity, 50%) was observed in six patients. Palliative
surgery was performed in three patients who had duodenal obstruction and other
CT findings indicating unresectability (superior mesenteric vein invasion or
liver metastasis), and therefore, thorough inspection of the superior
mesenteric vein was not possible. In another patient, radical surgery was
planned, but surgical inspection disclosed one solitary liver metastasis.
Therefore, palliative surgery was performed, and the superior mesenteric vein
was not explored. Two patients with more than 50% tumoral—vascular
contact were successfully resected but required venous resection in one case
and venous resection with graft placement in the other case
(Fig. 4).
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Thirty-three patients had no sign of superior mesenteric vein invasion (tumor-to-vessel contiguity, <50%). Eight patients had tumor-to-vein contiguity of less than 50%, suggesting no such invasion. Six of these patients were resected but did not undergo venous resection, and two patients were not evaluated because of palliative surgery. Twenty-five patients showed no tumor-to-vessel contact. In 23 of the patients, tumors could be resected. In two patients, the superior mesenteric vein was not evaluated because of palliative surgery
Portal vein.— Portal vein invasion (tumor-to-vessel contact,
50%) was detected in three patients. Two patients underwent palliative
surgery, and venous invasion was not evaluated. In the other patient, radical
surgery was planned, but surgical inspection disclosed regional lymph node
metastasis. Therefore, palliative surgery was performed, and the portal vein
was not explored.
In 32 patients, no tumor-to-vessel contact was observed. Of these, 25 patients underwent resection. In seven patients, palliative surgery was performed, and the portal vein was not evaluated. In three patients, helical CT did not reveal vascular invasion (tumor-to-to-vessel contact, <50%), but vascular invasion was found at surgery. Patients were successfully resected with venous resection (Fig. 5).
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Venous invasion as a whole (superior mesenteric vein and portal vein) was identified at surgery in 12 (30.8%) of the 39 patients. Helical CT had a sensitivity of 75% (9/12) in revealing venous invasion. Three patients (25%) with false-negative findings of less than 50% tumor-to-vein contiguity were found to have venous invasion at surgical exploration. The negative predictive value of helical CT to exclude venous invasion was 90%. One additional patient had venous resection because of surgically based suspicion of venous invasion, but microscopic examination showed no tumor invasion.
Periarterial streaks.—In eight patients, we detected reticular opacities or streaks radiating from the tumor and abutting the superior mesenteric artery without definite tumor-to-vessel contact. All these patients were surgically explored. Six of the patients were successfully resected (Fig. 6), and two patients were unresectable (Fig. 7). The positive predictive value of periarterial streaks for unresectability was 25% (2/8).
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Therefore, the main role of preoperative imaging is to distinguish between potentially resectable and clearly unresectable patients so that the optimal treatment for each patient can be ascertained. Various imaging procedures have been proposed for use in preoperative staging of pancreatic cancer, although no consensus has been reached concerning the best imaging algorithm.
Contrast-enhanced helical CT has been extensively used as a tool in both diagnosing and staging pancreatic adenocarcinoma [5,6,7,8], mainly focusing on metastatic spread to the liver and local invasion of vascular structures. The reported sensitivity of helical CT in revealing pancreatic carcinoma is high, ranging between 89% and 97% [4,6,8,9,10].
Metastatic liver disease is a well-accepted criterion of unresectability for pancreatic adenocarcinoma [11]. Detection of tiny metastatic liver lesions remains the most difficult part of preoperative staging of pancreatic cancer. In our series, 55% (5/9) of the false-negative findings for resectability were due to undetected liver metastasis. In addition, all patients with solid hepatic lesions larger than 1 cm were confirmed as having metastases. However, all patients excluded from surgery because of liver metastasis had several hepatic lesions, some of them larger than 2 cm.
In one (20%) of the five patients with liver metastasis, a hypervascular lesion in the pancreatic phase was seen retrospectively to correspond to a hypervascular metastasis (Fig. 3A,3B). However, this lesion would be difficult to differentiate from a small hemangioma. In addition, we missed two other tiny metastatic lesions found in this patient. In another patient, a tiny 1-cm hypodense lesion was detected in retrospect. In the other three patients, additional lesions were not found after careful retrospective evaluations. In each of these three patients, only one tiny metastatic lesion was found at surgical exploration. Therefore, metastatic pancreatic cancer might present as an isolated small solid lesion. In that clinical setting, if no other ancillary findings of unresectability are found, it would be necessary to perform diagnostic laparoscopy before excluding the patient from surgery.
In our series, preoperative nodal staging was clearly inaccurate. Only 16.6% of the patients with lymph node metastasis had the metastasis detected prospectively. This low detection rate is similar to those reported in previous studies [6, 9] and reflects the fact that size is not a discriminant feature between metastatic and nonmetastatic lymph nodes because a lymph node of normal size might be infiltrated by tumor. However, in clinical practice, the low detection rate of metastatic lymph nodes has a limited importance because most metastatic lymph nodes are resected at surgery.
Arterial invasion is another well-accepted criterion of unresectability [11]. However, peripancreatic venous invasion is a controversial contraindication for pancreaticoduodenectomy. Some surgeons believe that surgery is precluded in cases of tumor invasion of the portal vein or superior mesenteric vein, whereas other surgeons will perform aggressive surgery with mesenteric vein resection [4]. Recent surgical experience in resecting pancreatic adenocarcinoma with venous invasion has not shown histologic features suggesting a worse prognosis [12]. Therefore, assessment of major venous structures is a key factor in preoperative staging of pancreatic cancer and is critical for deciding surgical procedures. In fact, thorough assessment of mesenteric vessels during surgical exploration is extremely difficult because direct inspection of the lateral and posterior wall of mesenteric vessels can only be performed after gastric and pancreatic transections have been performed. At that point, resection is inevitable—either with negative margins or by cutting through the tumor [13]. Initial reports [14] with conventional CT suggested that any degree of tumor-to-vessel contiguity indicated unresectability of the tumor. However, our subject group mainly consisted of patients with advanced pancreatic cancer, and only seven patients had surgical correlations. Therefore, those vascular invasion criteria may not be applicable to the more limited forms of pancreatic cancer.
Recent reports have attempted to grade the degree of vascular invasion. Loyer et al. [7] proposed a classification of vascular involvement in pancreatic ductal adenocarcinoma that divided tumor-to-vessel contiguity into six types, ranging from type A, in which a fat plane is present between the tumor and the vessel, to type F, in which the tumor occludes the vessel. These authors found that 95% of the patients with types A and B were resectable without venous resection, whereas 47% of the patients with type D needed venous resection. Types E and F were unresectable in all cases, and type C was non-specific. This classification has the merit of being the first attempt to stratify patients with vascular invasion to distinguish the clearly unresectable patients from the potentially resectable patients. However, this classification is complex and relatively subjective and does not provide a clear cut-offs for resectable and unresectable patients. In addition, the authors do not differentiate between venous and arterial invasion. In another series, Lu et al. [15] studied 35 patients with pancreatic adenocarcinoma who underwent surgery. These researchers focused on local staging of pancreatic adenocarcinoma and developed a grading system for vascular tumor invasion on the basis of circumferential contiguity of the tumor to the vessel—from no contiguity to more than 75% circumferential involvement. These authors reported a sensitivity of 84% and a positive predictive value and negative predictive value for unresectability of 95% and 93%, respectively, when a threshold of 50% circumferential contiguity of tumor is used as a criterion of unresectability. The main limitation of this study is that only 11 patients were eventually resectable, and most of the surgical correlation was based on venous vessels. This particular limitation is of utmost importance because although venous invasion is a controversial contraindication for radical resection, arterial invasion is a well-accepted unresectability criterion.
In our series, arterial invasion was considered a formal contraindication for pancreaticoduodenectomy, and no patients with clear tumor-to-artery contiguity underwent surgery. Conversely, small reticular opacities arising from the tumor and abutting an arterial vessel are occasionally found in preoperative evaluation of pancreatic adenocarcinoma and may raise the question whether arterial invasion is present. We have seen these periarterial streaks in eight patients, all of whom were surgically explored; six patients could be resected, and two could not. Therefore, the positive predictive value of periarterial streaks for unresectability was only 25%. Thus, one cannot rely solely on this finding to exclude patients from surgery, although the surgeon must be made aware that in 25% of the cases, the patient will not be resectable.
The sensitivity of helical CT in showing portal or superior mesenteric vein invasion was 75% (9/12) in our series. Five of these patients were successfully resected after venous resection and end-to-end anastomosis in four cases and venous resection with venous graft in the remaining case. In addition, one patient had venous resection for suspected vascular invasion discovered at surgery that was found to be only fibrosis at histopathologic study. In our series, five (83%) of six venous resections had evidence of tumor invasion at micro-scopic examination. In contradistinction, in the series of Launois et al. [4], only 21% of venous resections showed definite tumor invasion of the venous wall. Because Launois et al. studied 445 patients over a 20-year period, the discrepancy between their rate of tumor venous invasion and ours might be related to our use of better preoperative staging techniques.
In conclusion, we find that helical CT used as the only preoperative imaging technique in pancreatic adenocarcinoma provides accurate pre-operative staging (positive predictive value for resectability of 77%). Local extension of pancreatic cancer and invasion of adjacent vascular structures are well depicted with dedicated thinsection helical CT. The main limitations of helical CT in preoperative staging are a difficulty in revealing unsuspected tiny liver metastases (55% of the false-negative findings for resectability) and a low rate of revealing lymph node metastasis (16.7%). Possibly, use of multidetector helical CT may improve our results in preoperative staging. Specifically, we believe that obtaining an arterial phase image of the liver before the pancreatic phase may improve the detection of tiny liver metastases. Our experience is that diagnostic endoscopic retrograde cholangiopancreatography is unnecessary in the diagnostic and preoperative workup of patients with suspected pancreatic cancer and should be reserved exclusively for palliative therapy in unresectable patients. In our institution, because of the noninvasiveness of the examination and its wide availability, helical CT has become the routine preoperative imaging technique in patients with suspected pancreatic adenocarcinoma.
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