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1
Department of Radiology, Faculty of Medicine, Kagoshima University, 8-35-1
Sakuragaoka, Kagoshima City, 890-8520, Japan.
2
Department of Second Pathology, Faculty of Medicine, Kagoshima University,
Kagoshima City, 890-8520, Japan.
Received June 14, 1999;
accepted after revision August 3, 1999.
Address correspondence to Y. Fukukura.
Abstract
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MATERIALS AND METHODS. Twenty-seven patients (nine with malignant and 18 with benign intraductal papillary-mucinous tumors) underwent thin-section (3- or 5-mm) helical CT. Two-phase enhanced CT was started 30 and 60-70 sec after injection of contrast material at 3 ml/sec.
RESULTS. In six patients (22.2%), a bulging papilla was depicted on CT. Twenty-five patients (92.6%) had a dilated main pancreatic duct. Cystic lesions were seen in 25 patients (92.6%). Thirteen lesions (48%) were located in the uncinate process, seven (25.9%) were in the head, two (7.4%) were in the body, and three (11%) were in the tail. The cystic lesion was unilocular in five patients (18.5%) and multilocular with a lobulated margin in 20 patients (74%). Communication between the main pancreatic duct and the cystic lesion was depicted in 19 patients (70.4%). The papillary projections corresponding to 3-mm or larger papillary neoplasms were depicted in five patients (18.5%). The bulging papilla was more often observed in malignant than in benign intraductal papillary mucinous tumors (p < 0.05). The caliber of the main pancreatic duct was significantly larger in patients with malignant intraductal papillary mucinous tumors (p > 0.001).
CONCLUSION. The most frequently found feature of intraductal papillary mucinous tumors was a lobulated multilocular cystic lesion located in the uncinate process and in contiguity with the dilated main pancreatic duct. In some patients, a bulging papilla and papillary projections in the ducts, which were specific findings, were visualized on CT. The bulging papilla and the caliber of the main pancreatic duct helped differentiate malignant from benign intraductal papillary mucinous tumors.
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Recently, helical CT with slip-ring technology has been used successfully for imaging the pancreas [17, 18, 19]. Helical CT offers some advantages compared with conventional CT. For example, images of the entire pancreas can be obtained during a single breath-hold with a slice thicknesses of 3-5 mm with excellent resolution of fine details such as the pancreatic duct [20].
The purpose of this study was to evaluate the thin-section helical CT findings of intraductal papillary mucinous tumors. More specifically, we wanted to determine whether helical CT could distinguish between malignant and benign intraductal papillary mucinous tumors.
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CT was performed on either Xvigor (Toshiba, Tokyo, Japan) or Xvision (Toshiba) equipment. One liter of contrast medium was given orally to 10 patients before CT. After unenhanced CT scans were obtained with 10-mm collimation of the liver and pancreas, 100 ml of the contrast medium (iohexol, Omnipaque 300; Daiichi, Tokyo, Japan) was infused into the antecubital vein at a rate of 3 ml/sec with a dedicated injector. Helical CT parameters included 5-mm collimation in 13 patients between 1994 and 1996 and 3-mm collimation in 14 patients between 1997 and 1998, 5- or 3-mm reconstruction intervals with 120 kVp, 230-250 mA, and a 1:1 table pitch. Two-phase helical CT scans were obtained at 30 and 60-70 sec after starting the infusion of contrast medium. First- and second- phase images were acquired during a single breath-hold, with a 10-sec interval for breathing between the two phases.
All CT images were interpreted by three radiologists who were aware of the intraductal papillary mucinous tumors but had no information regarding the endoscopic retrograde pancreatographic and histopathologic findings. Differences were resolved by a majority decision. The observers were asked to record the following information: the size of the long and short axis of the papilla within the duodenal lumen; the maximum caliber of the main pancreatic duct; the size, location (uncinate process, head, body, or tail), form (unilocular or multilocular) of the cystic lesion; the presence of a communication between the main pancreatic duct and the cystic lesion; the presence of a papillary projection into the main pancreatic duct or the cystic lesion; and the presence of infiltration within the pancreatic parenchyma or other organs. Imaging of the duodenal papilla by CT was correlated with the endoscopic retrograde pancreatographic findings. When a cystic lesion was visualized, the size of the largest loculus was measured. When a communication was visualized, the caliber of the communicating duct was measured. The presence of a cystic lesion and a communication duct were correlated with the endoscopic retrograde pancreatographic findings, the surgical specimens, or both. When the papillary projection in the main pancreatic duct or the cystic lesion was visualized on both first- and second-phase images, the highest papillary projection was measured. The presence of an altered contour of the pancreas, altered enhancement, or fistula formation was interpreted as evidence of infiltration into the pancreas or other organs. The presence of a papillary projection and infiltration on CT images was correlated with the histopathologic features.
Endoscopic studies from all patients were available for review. Each pancreatogram was evaluated for the presence of a cystic lesion in contiguity with the main pancreatic duct by two radiologists, with disagreements settled by consensus. The endoscopist's report of the presence of a bulging Vater's papilla on endoscopy was also noted.
Surgically resected pancreatic specimens were immediately fixed in 10% formalin and cut into serial 3- to 5-mm thick slices. We then prepared paraffin-embedded sections and stained them with H and E for histologic examination. The macroscopic and histologic findings underwent a blinded review. Communication between the main pancreatic duct and the cystic lesion was carefully observed and the highest papillary projection in the duct was measured.
The thin-section helical CT scans of 51 patients with other pancreatic diseases diagnosed on pathologic studies of surgical or biopsy specimens between 1993 and 1998 at our institution were also reviewed to assess the size of the papilla in the duodenal lumen by the same method. Thirty-one patients had pancreatic carcinoma, 10 had islet cell tumors, and five had chronic pancreatitis. One case was found of each of the following: a solid and cystic tumor, a serous cystadenoma, a mucinous cystadenoma, a lymphoepithelial cyst, and splenosis. These 51 patients formed a control group with a healthy duodenal papilla confirmed on endoscopic retrograde pancreatography. CT scans were obtained using the same scanner with contiguous 5-mm collimation on 24 patients between 1994 and 1996 or 3-mm collimation on 27 patients between 1997 and 1998. Eleven patients were given an oral contrast medium.
The presence of a bulging papilla, the caliber of the main pancreatic duct, the form and location of the cystic lesion, the communication, and the papillary projection were statistically evaluated with the chi-square test for comparison between malignant and benign intraductal papillary mucinous tumors. The unpaired Student's t test was used to compare the caliber of the main pancreatic duct, the size of the cystic lesion, and the loculus. A p value of less than 0.05 was considered statistically significant.
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The caliber of the main pancreatic duct ranged from 1 to 12 mm (mean, 6.2 mm). A main pancreatic duct of more than 3 mm in diameter was found in 25 patients (92.6%) and of more than 10 mm in diameter in six patients (22.2%) (Fig. 2A).
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On examination of the 27 surgical specimens, two patients with malignant intraductal papillary mucinous tumors had no cystic lesions, but the remaining 25 patients had such lesions. CT depicted a cystic lesion in all 25 patients (100%). The cystic lesion and the largest loculus ranged from 13 to 40 mm (mean, 24.7 mm) and from 5 to 23 mm (mean, 13.5 mm), respectively, in maximum diameter. Thirteen lesions (52%) were located in the uncinate process of the pancreas (Fig. 1B), seven (28%) were in the head, two (8%) were in the body, and three (12%) were in the tail (Fig. 3A). The cystic lesion was unilocular (Fig. 4) in five patients (20%) and multilocular with a lobulated surface (Figs. 1B and 3A) in 20 patients (80%).
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A communication between the main pancreatic duct and the cystic lesion was visualized on endoscopic retrograde pancreatography (Fig. 3B) in 20 of the 25 patients. In the remaining five patients, the communication was detected by examining surgical specimens (Fig. 1D). CT depicted the communication (Figs. 1C and 3A) in 19 (76%) of 25 patients with cystic lesions; the communicating duct ranged from 3 to 9 mm (mean, 4.5 mm) in diameter.
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Histopathologically, one patient had 3-mm papillary neoplasms in the cystic lesions, and two patients had 5-mm neoplasms projecting into the main pancreatic duct. Another two patients had 8-mm neoplasms projecting into the main pancreatic duct (Fig. 2C) and the cystic lesion. The remaining 22 patients had papillary neoplasms shorter than 3 mm (Fig. 1D). In all five patients with 3-mm or larger papillary neoplasms, CT scans depicted papillary projections in the main pancreatic duct or the cystic lesion (Fig. 2B). The papillary neoplasms shorter than 3 mm in the other 22 patients were not visualized on CT (Figs. 1B and 3A). Although invasion into the pancreatic parenchyma was histologically observed in seven patients with malignant intraductal papillary mucinous tumors (Fig. 2D), CT did not depict invasion in any of them (Fig. 2B).
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A bulging duodenal papilla was significantly more common in malignant than in benign intraductal papillary mucinous tumors (p < 0.05). The difference in the caliber of the main pancreatic duct between malignant and benign intraductal papillary mucinous tumors was also significant (p < 0.001). A significantly higher incidence of a main pancreatic duct of more than 10 mm in diameter was found among patients with malignant intraductal papillary mucinous tumors than among those with benign intraductal papillary mucinous tumors (p < 0.001). However, no significant differences were observed between the two groups with respect to the size, location, and form of the cystic lesions, the communications, and the papillary projections seen on CT scans.
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Most cystic lesions of the pancreas are pseudocysts, and cystic neoplasms represent 10-15% of pancreatic cysts [23, 24]. Cystic neoplasms were divided into microcystic tumors (or serous cystadenomas) and macrocystic tumors (or mucinous cystic tumors) by Compagno and Oertel [25]. An intraductal papillary mucinous tumor is a relatively new entity distinct from other pancreatic cystic neoplasms [1, 2]. It features duct segments that are filled with viscous mucin and that are lined by well-differentiated mucin-secreting cells forming papillary folds and occasionally showing cellular atypia [1, 7]. Many reports discuss the endoscopic retrograde pancreatographic characteristics of intraductal papillary mucinous tumor [3, 8, 10]. At endoscopy, a bulging papilla with mucin leaking through it is a specific finding [3, 8, 10, 11]. Endoscopic retrograde pancreatography reveals dilatation of the main pancreatic duct and the simultaneous opacification of a grapelike cystic lesion, which reflects the characteristic focal cystic dilation of the pancreatic ductal branches [3, 4, 11]. CT features of the papilla bulging into the duodenal lumen in patients with this tumor have been previously reported [4, 9], but the diagnostic criteria and percentage are still unclear. The results of our study suggest that a duodenal papilla smaller than 10 x 10 mm on CT scans is healthy. CT scans depicted a bulging papilla in 42.9% of the patients in whom this finding was seen during endoscopy. Although the rate of depiction of this feature on CT is low (22.2%), this finding may be important to differentiate intraductal papillary mucinous tumors from other pancreatic diseases.
Histopathologically, intraductal papillary mucinous tumor features ectasia of the main pancreatic duct or branch ducts, which are filled with viscous mucin. A dilated main pancreatic duct and a lobulated multilocular cystic lesion (grapelike cystic lesion) located in the uncinate process were the most frequent CT features in our study. This pattern was also reported previously [4, 8, 9, 10]. However, the features were not constant because they were not seen in 15 of our patients (55.6%). In two patients (7.4%), a healthy main pancreatic duct was found. Furthermore, two patients (7.4%) had no cystic lesions, and five patients (20%) with cystic lesions had unilocular cysts. In 12 patients (48%), the cystic lesion was not located in the uncinate process. Differentiating this entity from other cystic diseases or chronic pancreatitis is difficult in patients without the most frequent features. Unilocular cystic lesions are difficult to distinguish from pancreatic pseudocysts. If a cystic lesion is lobulated multilocular, however, it becomes difficult to differentiate from serous cystadenoma or a mucinous cystic tumor. This difficulty occurs because serous cystadenomas usually consist of small cystic spaces less than 2 cm in diameter [14, 26], and most of the largest loculi in our intraductal papillary mucinous tumors were also less than 2 cm in diameter. Mucinous cystic tumors are usually multilocular cystic lesions with a smooth surface, but a lobulated surface may be seen [13, 15]. A dilated main pancreatic duct without a cystic lesion may lead to the incorrect diagnosis of chronic pancreatitis.
In this respect, the presence of a communication between the main pancreatic duct and the cystic lesion is also one of the most reliable findings for the diagnosis of the intraductal papillary mucinous tumor on endoscopic retrograde pancreatography and MR cholangio-pancreatography [9, 11, 12]. In previous studies without thin-collimation or helical CT, it was difficult to recognize the communication [4, 8, 9, 10]. However, our method of thin-section helical CT depicted the communication in 19 patients (76%). Therefore, thin-section helical CT is useful for evaluation of the communication between the main pancreatic duct and the cystic lesion. Serous cystadenoma and mucinous cystic tumors do not usually communicate with the main pancreatic duct [6, 26]. Although pseudocysts often communicate with the main pancreatic duct, the size of the communicating duct is small [12]. We believe that detection on thin-section helical CT is more specific for intraductal papillary mucinous tumor because the visualized communicating duct was more than 3 mm in diameter.
The dilated ducts contain grossly visible papillary neoplasms and are lined by well-differentiated mucin-secreting cells forming papillary folds. On endoscopic retrograde pancreatography and CT, papillary projections into the main pancreatic duct or cystic lesions are also important for differentiating intraductal papillary mucinous tumors from pancreatic ductal cell carcinoma, serous cystadenoma, or pseudocysts [8, 9]. Mucinous cystic tumors also have papillary projections into the cystic lesions, but not into the main pancreatic duct [15]. To our knowledge, there have been no previous reports on the relationship between CT detectability and the height of papillary neoplasms. In our study, papillary projections in the ducts were seen in five patients (18.5%). Thin-section helical CT was useful for detecting papillary neoplasms that were 3 mm or larger.
The prognosis of this disease is worse in patients with invasive carcinoma than in patients without invasion [1, 5]. In patients with invasion, radical dissection of the lymph nodes is necessary [5]. Therefore, it is important to diagnose invasion into the pancreatic parenchyma or other organs in planning the treatment. Invasion into the pancreatic parenchyma was not depicted on CT in any of our patients because all of them had chronic pancreatitis and the invasion was minimal.
It is important to differentiate between malignant and benign intraductal papillary mucinous tumors because some intraductal papillary mucinous tumors are not malignant and can be followed up later [5]. In this study, a bulging papilla was more often observed in malignant than in benign intraductal papillary mucinous tumors. The difference in the caliber of the main pancreatic duct between malignant and benign intraductal papillary mucinous tumors was significant. This result is consistent with those of other studies; Kimura et al. [5] reported that benign intraductal papillary mucinous tumors were significantly more common in patients in whom the main pancreatic duct was not dilated. Itoh et al. [4] reported that seven of nine patients with dilatation of the entire main pancreatic duct on endoscopic retrograde pancreatography and CT had malignant epithelium, whereas all three patients with no or focal dilatation of the main pancreatic duct did not have malignant epithelium. Moreover, in our study, all patients with a main pancreatic duct more than 10 mm in diameter had a malignant epithelium. Kimura et al. also reported that a malignant intraductal papillary mucinous tumor was significantly more common in patients with a cystic lesion larger than 6 cm. However, our patients had no cystic lesions larger than 6 cm, and no significant difference between the two groups with respect to the cystic lesions was found. This point should be clarified in future studies.
In conclusion, the most frequently seen feature of intraductal papillary mucinous tumors is a lobulated multilocular cystic lesion that is located in the uncinate process and is in continuity with the dilated main pancreatic duct. In some patients, a bulging papilla and papillary projections in the duct, which are specific findings, are visualized on thin-section helical CT. The bulging papilla and the caliber of the main pancreatic duct may be helpful to differentiate malignant from benign intraductal papillary mucinous tumor.
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