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CT and Pathologic Assessment of Prospective Nodal Staging in Patients with Ductal Adenocarcinoma of the Head of the Pancreas

¹ Department of Radiology, Royal Liverpool University Hospital, Prescot St., Liverpool, L7 8XP, United Kingdom.
² Department of Pathology, Royal Liverpool University Hospital, Liverpool, L7 8XP, United Kingdom.
³ Department of Surgery, Royal Liverpool University Hospital, Liverpool, L7 8XP, United Kingdom.

Received September 24, 2001; accepted after revision July 11, 2002.

 
Address correspondence to M. L. Hughes.

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. The aim of our study was to compare the assessment of peripancreatic lymph nodes using CT with the gold standard of detailed histopathologic assessment of resected specimens in patients with pancreatic ductal adenocarcinoma.

SUBJECTS AND METHODS. Sixty-two patients with presumed pancreatic carcinoma were prospectively studied with dual-phase contrast-enhanced helical CT, and images were interpreted in consensus by three radiologists. Complete surgical resection was performed in 28 patients. A detailed nodal classification system was used for radiologic, surgical, and pathologic staging in the nine patients whose final diagnosis at histology was pancreatic ductal adenocarcinoma.

RESULTS. Forty lymph nodes were prospectively identified on CT in these nine patients. Two of 23 nodes (9%) measuring less than 5 mm in the short-axis diameter were malignant, four of 11 nodes (36%) measuring 5-10 mm were malignant, and one of six nodes (17%) larger than 10 mm was malignant. Using a short-axis diameter of greater than 10 mm as the criterion for nodal involvement, we found a sensitivity of 14% (1/7) and a specificity of 85% (28/33), with a positive predictive value of 17% (1/6), a negative predictive value of 82% (28/34), and an overall accuracy of 73% (29/40). Ovoid nodal shape, clustering of nodes, and the absence of a fatty hilum were not useful predictors of malignancy on CT.

CONCLUSION. In resectable pancreatic ductal adenocarcinoma, CT is not accurate overall for the prediction of nodal involvement. In a patient with presumed pancreatic carcinoma that is considered to be resectable, the depiction on CT of peripancreatic nodes should not prevent attempted curative resection.

Introduction

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Pancreatic carcinoma is among the leading causes of cancer deaths [1,2,3]. The prognosis of pancreatic carcinoma is dismal [1, 2, 4,5,6,7]. Less than 20% of patients are alive at 1 year after diagnosis, and the average 5-year survival rate is 0.4% [1, 4, 6, 8]. Only 3-22% of tumors are resectable at presentation [1, 3, 4, 8,9,10], making pancreatic carcinoma the least likely cancer to be confined to the organ of origin at the time of diagnosis [2, 7].

The preoperative diagnosis of pancreatic carcinoma is based on clinical presentation, tumor markers, and diagnostic imaging tests but not on histology or cytology. Histologic findings of the resected specimens often show a range of diagnoses, including both benign and malignant tumors and chronic pancreatitis. These findings are acceptable to the surgeon whose aim is to resect a tumor presumed before surgery to be a pancreatic cancer. Accurate tumor staging is important in selecting patients for attempted curative surgery. CT has proven accurate in the identification of those patients whose disease is advanced and unresectable [2, 4, 11] but performs less well in the evaluation of local extension in patients with potentially resectable tumors [2, 4, 6, 10]. Many patients undergo laparotomy only to be found to have unresectable disease [2, 12]. Although CT is useful in the assessment of vascular involvement and metastatic spread, its accuracy for nodal staging is unproven.

We undertook a prospective study to determine the accuracy of dual-phase helical CT in the prediction of metastatic lymph node involvement in patients with pancreatic carcinoma using a detailed nodal classification described by the Japan Pancreas Society [13] (Table 1). The Japan Pancreas Society nodal classification was used throughout the study to describe the radiologic, surgical, and pathologic findings. We used the International Union Against Cancer (UICC) TNM classification [14] for overall tumor staging.

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1. —Diagram shows Japan Pancreas Society [13] nodal group locations in pancreatic cancer. Node classifications and corresponding locations are detailed in Table 1. SMV = superior mesenteric vein, SMA = superior mesentric artery.

Top Abstract Introduction Subjects and Methods Results Discussion References

In all patients, the presumptive diagnosis of pancreatic carcinoma was based on clinical symptoms, laboratory findings (including tumor markers), and results of endoscopic retrograde cholangiopancreatography or sonography. All potentially eligible patients underwent dual-phase helical CT of the pancreas and staging laparoscopy, including laparoscopic sonography.

Patients were excluded from further analysis for the purposes of this study if findings on CT or laparoscopic sonography showed that the tumor was not resectable by criteria of proven metastasis or vascular occlusion. Of the 62 patients enrolled in the study, 28 patients underwent full resection with radiologic and pathologic correlation. Nine patients with pancreatic ductal adenocarcinoma (three men and six women; age range, 53-78 years; mean age, 67 years) composed our study population.

Standard of Reference
The standard of reference was the histopathologic assessment of resected lymph nodes in patients whose final histologic diagnosis was pancreatic ductal adenocarcinoma.

CT Imaging Parameters
After preliminary unenhanced axial scans were acquired for localization, dual-phase helical CT scanning was performed (HiSpeed Advantage scanner; General Electric Medical Systems, Milwaukee, WI). An IV bolus of at least 100 mL of iopromide (Ultravist 300; Schering, Berlin, Germany) was administered via a pump injector at 3 mL/sec. The first phase through the pancreas began at 30 sec after initiation of the bolus, and 3-mm slices were obtained using a pitch of 2 to optimize visualization of the primary tumor, peripancreatic nodes, and vessels. The second phase began at 75 sec after initiation of the bolus, with 5-mm slices obtained using a pitch of 2 to cover the liver and pancreas—mainly to show liver metastases. Dilute meglumine diatrizoate (2%) (Gastrografin; Schering, Berlin, Germany) was administered orally to opacify the stomach and duodenum.

Image Analysis
Three experienced radiologists interpreted each CT scan before the histologic diagnosis was made. The observers were unaware of all other investigations, and agreement was reached by consensus. Analysis involved evaluation of the primary tumor characteristics, vessel encasement, stenosis or invasion (including the superior mesenteric—portal venous system and the superior mesenteric, splenic, and hepatic arteries), and assessment of distant metastases.

Particular attention was paid to nodal involvement, especially specific node groups as described by the Japan Pancreas Society (Table 1 and Fig. 1). Nodes were measured and categorized into three groups by short-axis diameter: less than 5 mm, 5-10 mm, and greater than 10 mm. The observers commented on nodal morphology, including ovoid versus spherical shape, whether or not the nodes appeared in clustered groups of three or more, and the presence or absence of a lucent fatty hilum. For the purposes of TNM classification, only lymph nodes with a short-axis diameter greater than 10 mm were considered positive; morphology was not used for staging.

After the TNM classification was determined, each tumor was labeled as resectable or unresectable on the basis of CT findings. Criteria for unresectability included peritoneal metastases, liver metastases, or ascites; extrapancreatic invasion of adjacent tissues and organs other than the duodenum or bile duct; and occlusion or stenosis of the major pancreatic vessels. Encasement of the portal vein was not considered a deterrent to attempted curative surgery, provided that less than half of the vessel circumference and less than 1 cm of its length were affected. The presence of enlarged lymph nodes per se, in the absence of any other evidence of unresectability, was not considered a contraindication to attempted resection.

Laparoscopy and Laparoscopic Sonography
Using findings from laparoscopy and laparoscopic sonography, we assessed the size and extent of tumor, including vascular involvement, the presence and size of lymph nodes, and liver metastases. The tumors were then labeled as resectable or unresectable.

Surgery
The surgeons were aware of the study design and the necessity to accurately label all specimens. In particular, lymph node specimens were identified according to the Japan Pancreas Society classification (Table 1 and Fig. 1). The site and extent of tumor, including local invasion, local vessel involvement (encasement, stenosis, or invasion, and the need for portal vein resection), and the presence or absence of liver or other metastases, were noted at surgery. Patients deemed to have resectable disease underwent a standard Kausch-Whipple pancreatoduodenectomy [1, 15]. Regional lymph nodes were dissected according to the Japan Pancreas Society classification. The lymph node groups removed en bloc with the resection specimen were 13a and b, 17a and b, 12b1, 12b2, 12c, 14a and 14b [13, 15]. For the purposes of the study, group 8a and group 16b nodes were also resected and labeled individually [13].

Pathologic Evaluation
One pathologist with a special interest in pancreatic carcinoma examined all pathologic specimens. The pathologist was unaware of the results of all other investigations. The lymph nodes were dissected from the specimen, and the specimen and nodes were examined separately. Resected lymph nodes were identified individually according to the Japan Pancreas Society classification, and a TNM classification was determined.

Statistics
Categoric variables were compared using the chi-square test, and statistical significance was set at a p value of less than 0.05.

Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Of the 62 patients enrolled in the study, 24 had unresectable tumors on preoperative assessment, one died from unrelated causes before surgery could be performed, and two were considered unfit to undergo major surgery. In the remaining 35 patients, surgical exploration was done with a view to performing pancreatoduodenectomy with curative intent. At surgery, seven patients were found to have unresectable tumors (six pancreatic carcinoma, one gallbladder carcinoma). The remaining patients underwent a standard pancreatoduodenectomy. Histologic diagnoses in these 28 patients were pancreatic ductal adenocarcinoma (n = 9), intrapancreatic bile duct adenocarcinoma (n = 6), ampullary adenocarcinoma (n = 4), chronic pancreatitis (n = 4), microcystic adenoma (n = 2), mucinous cystadenoma (n = 1), intraductal papillary mucinous tumor (n = 1), and villous adenoma of the ampulla of Vater (n = 1).

Predictive Accuracy of CT Lymph Node Staging
A total of 513 nodes were identified (median, 18 nodes per resected specimen) in the 28 patients who underwent full resections. One hundred and nineteen of these nodes were prospectively identified on CT (mean, 4 nodes per patient) (Figs. 2 and 3). Sixty-nine of the 119 nodes measured 0-5 mm in the short-axis diameter, 41 were larger than 5 mm up to 10 mm, and nine were larger than 10 mm. We found no statistical difference in the number of nodes identified per patient in patients with pancreatic adenocarcinoma compared with those in patients with other histologic diagnoses, both benign and malignant.

View larger version (132K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2. —73-year-old man with pancreatic ductal adenocarcinoma. CT scan shows round 12-mm node (arrow) anterior to common hepatic artery (Japan Pancreas Society [13] group 8a). Histologic findings showed ductal adenocarcinoma metastases in this node

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3. —78-year-old woman with pancreatic ductal adenocarcinoma. CT scan shows ovoid 7-mm node (Japan Pancreas Society [13] group 8a, thick arrow) anterior to common hepatic artery and 6-mm node (Japan Pancreas Society group 13a, thin arrow) behind pancreatic head. Both were proven to be metastatic nodes.

In the nine patients with pancreatic adenocarcinoma who underwent resection, a total of 159 nodes were identified (median, 18 nodes per resected specimen). All nine patients were found to have nodal metastases at histology. Forty of the 159 nodes were identified prospectively on CT (median, 4 nodes per patient). Of these 40 nodes, two of 23 nodes (9%) measuring 0-5 mm were malignant, four of 11 nodes (36%) larger than 5 mm up to 10 mm were malignant, and one of 6 nodes (17%) larger than 10 mm was malignant (not statistically significant; ² = 3.949, p = 0.1388). Using a short-axis diameter of greater than 10 mm as our criterion for nodal involvement resulted in a sensitivity of 14% (1/7) and a specificity of 85% (28/33). The positive predictive value was 17% (1/6), the negative predictive value was 82% (28/34), and the overall accuracy was 72.5% (29/40). Reducing the size criterion for involvement to greater than 5 mm increased the sensitivity to 71% (5/7) but reduced the specificity to 64% (21/33). Using the 5-mm criterion, we found positive and negative predictive values of 29% (5/17) and 91% (21/23), respectively, and overall accuracy of 65% (26/40).

Twenty-two of the 119 nodes that were identified on CT contained metastases. In terms of detecting metastatic nodes, CT had a sensitivity of 24% (7/29), a specificity of 75% (97/130), a positive predictive value of 17% (7/40), a negative predictive value of 81% (97/119), and overall accuracy of 65% (104/159).

Regarding nodal morphology on CT, nodes less than 10 mm in short-axis diameter were classified as suspicious for involvement if the nodal shape was round rather than avoid, if nodes appeared in clustered groups of three or more, or if the normal fatty hilum of the node was not visible. On the basis of their shape, 10 of the 11 nodes measuring 5-10 mm were classified as suspicious; only four (36%) were proven malignant. The solitary ovoid node of this size was benign. Clustered lymph nodes were observed in three other patients; in all cases, the histologic findings of these nodes were benign. A fatty hilum was seen in only a single node, which was found to be benign at histology.

Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Pancreatic carcinoma is characterized by early spread beyond the pancreas with the development of subclinical metastases [7]. The challenges, therefore, are to obtain an early diagnosis and accurate tumor staging. CT is useful in determining unresectability, with a reported range of accuracy of 92-100% [2, 6, 11, 16]. CT has been of limited use, however, in determining resectability, with reported accuracies of 45-73% [6, 10, 11, 17], largely because of undetected subtle vascular invasion and small metastases in the liver and peritoneum. The incidence of nodal metastases in patients with pancreatic carcinoma is high. In other studies, 33-77% of patients with presumed resectable disease have subsequently been found to have nodal metastases [4, 7, 10, 11, 15, 18,19,20,21,22]; in our study, this figure was 100% (9/9 patients). In addition, a study using molecular analyses for mutant K-ras oncogene in resected lymph nodes indicates that approximately two thirds of patients with histologically negative lymph nodes may harbor micrometastases [23]. The presence of lymph node metastases adversely influences survival [17, 18], and 10-33% of patients who undergo extended resections have metastases in lymph nodes that are not included in a standard Kausch-Whipples resection [15, 20, 24, 25]. The addition of extended lymphadenectomy and retroperitoneal soft-tissue clearance does not appear to significantly increase morbidity or mortality [20, 25].

Studies assessing the accuracy of CT in pancreatic carcinoma have largely concentrated on local tumor staging, presence of vascular encasement, and determination of resectability, with CT findings being compared with findings at surgery [4, 5, 9,10,11,12, 16, 22, 26]. With regard to identification of nodal metastases, using CT produces poor results, largely because size criteria are used to determine nodal involvement. Normal-size lymph nodes often harbor micrometastases, and many enlarged lymph nodes are reactive [3, 4, 5, 7, 27]. Therefore, it seems inevitable that the accuracy of CT in nodal staging is limited. Table 2 summarizes the results of published studies in which figures for nodal staging are given. Our study shows sensitivity (14%), specificity (85%), and positive predictive values (17%) comparable to those reported in the literature. The negative predictive value (82%) and overall accuracy (72.5%) were higher in our study than in previously reported studies. Most investigators have used a short-axis diameter of 10 mm for diagnosing nodal involvement [5, 8, 26,27,28,29], but other investigators have chosen diameters of 5 mm [10], 15 mm [3, 17], or 20 mm [30]. All previous studies have used patients with pancreatic adenocarcinoma with the result that (as in our consecutive resection series) they invariably include patients with intrapancreatic bile duct, ampullary and duodenal, and other adenocarcinomas that are not pancreatic ductal in origin. Examination of the resection specimen is the only way to identify the exact cancer type and enable the precise identification of lymph nodes to determine whether they are involved.

In our referral group of 62 patients, 28 underwent a full resection procedure but only nine of these had pancreatic ductal adenocarcinoma. The small number of patients in this prospective study limits the statistical power of our results.

To our knowledge, ours is the first study to assess the accuracy of CT in nodal staging on a detailed, named, node-by-node basis using pathologic examination of resected nodes as the gold standard. Prior studies have assessed the accuracy of CT by means of surgery (a combination of laparotomy, biopsy, and resection without specifying the cellular origin of the cancer) and histology using a global nodal staging system. Given that enlarged nodes may be negative and normal-size nodes may be positive for metastases in pancreatic carcinoma, a global nodal staging system will be inaccurate if detailed radiologic—pathologic correlation is not undertaken. Unlike researchers whose study used sonography [28], we did not find that consideration of nodal morphology on CT increased the accuracy in detection of nodal metastases.

Pathologic correlation with CT in our study was performed to a degree of accuracy that, to our knowledge, has not previously been reported, and we have confirmed earlier reports that prospective nodal staging on CT is inaccurate. A detailed knowledge of peripancreatic nodal sites is essential, and a recognized classification system such as that of the Japan Pancreas Society is useful and can easily be used in CT analysis. Such a standardized classification is essential if different treatment strategies for pancreatic tumors are to be compared [15]. In a patient with a presumed pancreatic carcinoma that is considered to be otherwise resectable, the depiction on CT of enlarged peripancreatic or distant nodes should not be considered a contraindication to surgery—especially given the improving long-term results from adjuvant chemotherapy [31, 32].

In conclusion, CT is not accurate overall for the prediction of nodal involvement in resectable pancreatic ductal adenocarcinoma. In a patient with presumed pancreatic carcinoma that is considered to be resectable, the depiction on CT of peripancreatic nodes should not prevent attempted curative resection.

Acknowledgments
 
We thank the Department of Medical Illustration at the Royal Liverpool University Hospital for preparation of the images.

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