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Early Bile Duct Carcinoma: Comparison of Imaging Features with Pathologic Findings¹

¹ From the Departments of Radiology (J.H.L., D.C., W.J.L., H.K.L.) and Pathology (K.T.J.), Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Ilwon-dong, Kangnam-ku, Seoul 135-710, Korea. Received December 12, 2004; revision requested February 7, 2005; revision received February 15; accepted March 15; final version accepted April 18. Address correspondence to J.H.L. (e-mail: jhlim{at}smc.samsung.co.kr).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Purpose: To retrospectively evaluate the imaging features of early bile duct carcinoma and to compare these features with histopathologic findings.

Materials and Methods: The institutional review board did not require its approval or informed patient consent for this study. Twenty-one patients (13 men, eight women; mean age, 60 years; range, 48–75 years) with early bile duct carcinoma that was surgically resected and histopathologically confirmed were included. Ultrasonography (US) was performed in 15 patients, computed tomography (CT) in 21, cholangiography in 18, and magnetic resonance (MR) cholangiography in six. Two radiologists retrospectively reviewed imaging features by consensus; they compared growth pattern of tumors, integrity of the bile duct wall that harbored the tumor, and periductal infiltration with histopathologic findings.

Results: Pathologic specimens showed intraluminal tumor growth in all cases. Tumors were confined to the mucosa in 11 patients and involved the fibromuscular layer in 10 patients. In four of the 10 intrahepatic cholangiocarcinomas, four of the five hilar cholangiocarcinomas, and six of the six extrahepatic cholangiocarcinomas, there were intraductal tumor masses and the wall of the tumor-bearing bile ducts was preserved without periductal infiltration on US and CT images. On cholangiograms and MR cholangiograms, tumors were better delineated but the wall invasion could not be evaluated. No difference in image findings was found between carcinoma confined to the mucosa and carcinoma involving the fibromuscular layer.

Conclusion: Imaging features of early bile duct carcinoma are a tumor mass in the bile duct lumen and integrity of the tumor-bearing bile duct wall without infiltration outside the wall.

© RSNA, 2006

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Early bile duct carcinoma is defined as carcinoma limited to the mucosa or fibromuscular layer of the bile duct (1,2). With few exceptions, these tumors have no lymph node metastasis, venous invasion, or perineural or lymphatic infiltration. Patients with early bile duct carcinoma who undergo resection have an excellent prognosis. The cumulative 5-year survival rate is estimated as 83%–100% (1–5).

Sporadic reports have been issued regarding early bile duct carcinoma, described as early bile duct carcinoma (5), carcinoma confined to the mucosa (6), superficially spreading mucosal carcinoma of the bile duct (7), or intrabile duct carcinoma (8). More than 130 cases of early bile duct carcinoma have been reported in the Japanese literature (7), and clinical findings were described. However, most of the cases were diagnosed after surgery according to histopathologic examination, and imaging findings were not described. To our knowledge, one report has been published in which the imaging findings of early bile duct carcinoma (9) were described. Therefore, the purpose of this study was to retrospectively evaluate the imaging features of early bile duct carcinoma and to compare these features with histopathologic findings.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patients
There were 23 cases of early bile duct carcinoma among the 742 patients with intrahepatic or extrahepatic cholangiocarcinoma who were treated surgically in our institution from June 1994 to September 2004. Two patients with early bile duct carcinoma were excluded because images were impossible to evaluate as a result of a considerable amount of air and foodstuff in the bile ducts caused by a biliary-enteric fistula or concomitant bile duct stone and cholangitis. Twenty-one patients (13 men, eight women; mean age at diagnosis, 60 years; range, 48–75 years) with early bile duct carcinoma were thus included in our study. Fifteen patients underwent ultrasonography (US), all 21 patients underwent computed tomography (CT), 18 patients underwent cholangiography (endoscopic retrograde cholangiography in 15 patients, percutaneous transhepatic cholangiography in one, drainage tube cholangiography in one, and surgical cholangiography in one), and six patients underwent magnetic resonance (MR) cholangiography. The institutional review board at our institution did not require its approval or informed patient consent for this retrospective study.

Image Methods
Routine transabdominal hepatobiliary and pancreatic US examinations were performed in supine and right anterior oblique positions. Four gastrointestinal radiologists (including J.H.L., D.C.) who had 14, 3, 6, and 2 years of experience in hepatobiliary US at the commencement of study recruitment; three gastrointestinal radiology fellows; and three radiology trainees with the supervision of the aforementioned radiologists were involved in performing US examinations. All scans were obtained with commercially available high-end US units (XP 10, XP 4, or Sequoia 512, Acuson, Mountain View, Calif; UM9 or HDI 3000, 3500, or 5000, Advanced Technology Laboratories, Seattle, Wash; Logic 700, GE Medical Systems, Milwaukee, Wis) and 2–5-MHz probes. Endoscopic US was not performed.

CT imaging was performed before and after contrast agent administration with single–detector or multi–detector row CT scanners (HiSpeed Advantage, Lightspeed QX/i, Lightspeed Ultra, or Lightspeed 16; GE Medical Systems) as cases were collected over a 10-year period. Precontrast CT scanning was performed by using 7.5–10.0-mm section thickness and 7.5–10.0-mm intervals. With use of bolus-triggered technique, scanning during the late arterial phase began 45 seconds after the start of injection of 120 mL of nonionic iodinated contrast material (iopamidol, Iopamiro 300; Bracco, Milan, Italy) through the antecubital vein at a rate of 4 mL/sec, with 2.5–5.0-mm section thickness and 2.5–5.0-mm intervals. The portal phase of scanning began 70 seconds after the start of contrast material injection with 5-mm section thickness and 5-mm intervals.

MR cholangiopancreatography was performed with a 1.5-T superconducting MR imaging unit (Horizon; GE Medical Systems) with a phased-array multicoil system. Coronal heavily T2-weighted fast spin-echo images were obtained with the following parameters: repetition time msec/effective echo time msec, 5000/120–140; echo train length, eight to 12; field of view, 34–38 x 30–34 cm; section thickness, 3 mm; no intersection gap; matrix size, 256–512 x 128–192; fat saturation; number of signals acquired, two; acquisition time, 3–4 minutes. Coronal single-projection images and multislab thin-section images were obtained by using a single-shot fast spin-echo sequence with the following parameters: /160–200 with acquisition time of 2–3 seconds for the single projection and /90–100 with acquisition time of 82–104 seconds for the multislab projection; thick-slab thickness was 4–8 cm. Other parameters were the same as those used with the fast spin-echo technique. All sequences were performed by using respiratory triggering without breath holding. By using coronal multislab fast spin-echo and single-shot fast spin-echo sequences, source images were processed on a console using maximum intensity projection reconstruction, including target volume maximum intensity projection.

Endoscopic retrograde cholangiopancreatography was performed with an Evis duodenoscope (JF-200; Olympus, Tokyo, Japan). Ionic contrast material (meglumine iothalamate, 60%; Bracco) was used after 50% dilution. Tube cholangiography was performed with a nasobiliary catheter, percutaneous needle, or biliary catheter for bile drainage in patients with severe bile duct stenosis or obstruction. Endoscopy was performed by two gastroenterologists who had more than 3 years of experience with the technique. Five gastrointestinal radiologists (including J.H.L., D.C., W.J.L., H.K.L.) who had 14, 3, 5, 5, and 6 years of experience in hepatobiliary radiology at the commencement of study recruitment; six gastrointestinal radiology fellows; and five radiology trainees under the supervision of the aforementioned five radiologists were involved in performing cholangiography.

Image Interpretation
In this study, two gastrointestinal radiologists (J.H.L. and D.C.) with 24 and 6 years of experience in hepatobiliary imaging reviewed the US, CT, cholangiographic, and MR cholangiographic images in one interpretation session. All images were reviewed on a 2000 x 2000 picture archiving and communication system monitor (GE Medical Systems Integrated Imaging Solutions, Mt Prospect, Ill) with adjustment of optimal window settings and stack-view system if needed. Before image interpretation, these reviewers were aware that the patients had early bile duct carcinoma, but they did not know the detailed pathologic findings. In retrospective review, images were read at the same time; the reviewers did not try to evaluate the features separately from each modality without knowing what the other imaging modalities showed in the same patient. Decisions regarding imaging features were determined by consensus.

Two radiologists evaluated bile duct tumors in terms of the growth pattern, degree of contrast enhancement, depth of wall invasion, and periductal infiltration. The radiologists paid special attention to the presence of an intraductal mass; the integrity of the bile duct wall, that is, preservation of the echogenic line on US images and of the enhancing thin wall on CT images, especially at the site of the mass; and the periductal infiltration on CT images. When the echogenic line of the tumor-bearing bile duct wall was preserved on US images and a thin extrahepatic bile duct wall with a clear smooth margin was preserved on CT images, we considered the findings to be consistent with early bile duct carcinoma. A radiologist (J.H.L.) measured the attenuation value of the tumor mass on precontrast and postcontrast portal phase CT images. On CT images, we evaluated enlargement of the lymph nodes and distant metastases to the liver and bases of the lung. Cholangiograms and MR cholangiograms were evaluated for tumor size, shape, and location; extent of bile duct contour; and presence of mucin. We also evaluated bile duct stenosis or obstruction and dilatation of the duct proximal to the tumor.

Pathologic Evaluation
Pathology reports were available for all patients. A pathologist (K.T.J.) with 4 years of subspecialty experience in the biliary system and pancreas evaluated the histopathologic characteristics of the resected specimens regarding tumor morphology and the depth of bile duct wall involvement. When the tumor cells were limited to the mucosa or fibromuscular layer (stage T1 according to TNM system), the carcinoma was regarded as early; when tumor cells invaded the adventitia or outside of the wall or adjacent organs (stage T2 according to TNM system), the carcinoma was regarded as advanced (1,2). Tumor location, shape, and size; thickness of tumor-bearing bile duct wall; depth of tumor invasion; and tumor histologic type were analyzed. The lymph nodes obtained at surgery were examined.

Comparison of Imaging Features and Pathologic Findings
The results of imaging features were directly compared with pathologic findings by two radiologists (J.H.L. and D.C.). Particular attention was paid to the integrity of the tumor-bearing bile duct wall on images, and these images were compared with histopathologic findings with regard to the depth of tumor invasion into the wall of the bile duct and periductal infiltration.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Pathologic Findings
According to examination of surgical specimens, there were intraductal tumors in all patients. Tumors were located in the intrahepatic ducts in 10 cases, hilar in five, and extrahepatic in six (proximal extrahepatic duct in two cases, middle extrahepatic in one, both proximal and middle extrahepatic in one, and distal extrahepatic in two) and manifested as nodular mass in two patients, polypoid mass in 10, and castlike in nine. The size of tumors ranged from 1.1 to 5.5 cm in greatest diameter (mean, 2.9 cm). Ten tumors were less than 3 cm long, and 11 tumors were longer than 3 cm. Eleven tumors were located in the mucosal layer, and 10 tumors involved the fibromuscular layer but did not penetrate the entire wall. No patients had periductal infiltration or invasion into the adjacent hepatic or pancreatic tissue. Tumor histologic types were papillary adenocarcinoma in 13 patients, well-differentiated tubular adenocarcinoma in six, and well-differentiated papillotubular adenocarcinoma in two. There was no difference in the size of tumors between papillary carcinomas and tubular carcinomas. The tumor-bearing fibromuscular layer was thickened, the thickness varying from 1.5 to 2.0 mm. In one patient, there was lymph node metastasis in one of the porta hepatis lymph nodes at pathologic examination.

US Features
US images showed an intraductal soft-tissue mass with well-defined echogenic lines of the bile duct wall in one intrahepatic cholangiocarcinoma, three hilar cholangiocarcinomas, and six extrahepatic cholangiocarcinomas (Figs 1–3). The bile duct wall was more echogenic than the intraductal tumor. On transverse scans of the bile ducts obtained in two of the six patients with extrahepatic cholangiocarcinoma, circular or curved lines of outer margins were well delineated. In three intrahepatic cholangiocarcinomas, tumor mass was visualized but the echogenic lines of the bile duct wall were not delineated. In two patients, tumor mass was not depicted.

View larger version (164K): [in this window] [in a new window] [Download PPT slide]   Figure 1a: Images in a 64-year-old man with well-differentiated tubular adenocarcinoma of the right intrahepatic duct confined to mucosa. (a) Subcostal transverse transabdominal US image of the liver shows a castlike intraductal mass in the upper part of right hepatic lobe. Note intact echogenic lines of the bile duct wall (arrows). (b, c) Transverse contrast-enhanced arterial phase CT images show intraductal mass filling bile ducts like a cast. Note intact wall of the bile ducts (arrow). Percutaneous transhepatic cholangiogram (not shown) demonstrated severe dilatation of anterior segmental ducts of the right hepatic lobe and obstruction by intraductal tumor. (d) Micrograph of the specimen shows castlike tumor (stars) originating from and confined to mucosa filling the bile duct lumen. No tumor extends through the thickened fibromuscular layer of the duct wall (between arrows). L = liver parenchyma. (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (65K): [in this window] [in a new window] [Download PPT slide]   Figure 1b: Images in a 64-year-old man with well-differentiated tubular adenocarcinoma of the right intrahepatic duct confined to mucosa. (a) Subcostal transverse transabdominal US image of the liver shows a castlike intraductal mass in the upper part of right hepatic lobe. Note intact echogenic lines of the bile duct wall (arrows). (b, c) Transverse contrast-enhanced arterial phase CT images show intraductal mass filling bile ducts like a cast. Note intact wall of the bile ducts (arrow). Percutaneous transhepatic cholangiogram (not shown) demonstrated severe dilatation of anterior segmental ducts of the right hepatic lobe and obstruction by intraductal tumor. (d) Micrograph of the specimen shows castlike tumor (stars) originating from and confined to mucosa filling the bile duct lumen. No tumor extends through the thickened fibromuscular layer of the duct wall (between arrows). L = liver parenchyma. (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (71K): [in this window] [in a new window] [Download PPT slide]   Figure 1c: Images in a 64-year-old man with well-differentiated tubular adenocarcinoma of the right intrahepatic duct confined to mucosa. (a) Subcostal transverse transabdominal US image of the liver shows a castlike intraductal mass in the upper part of right hepatic lobe. Note intact echogenic lines of the bile duct wall (arrows). (b, c) Transverse contrast-enhanced arterial phase CT images show intraductal mass filling bile ducts like a cast. Note intact wall of the bile ducts (arrow). Percutaneous transhepatic cholangiogram (not shown) demonstrated severe dilatation of anterior segmental ducts of the right hepatic lobe and obstruction by intraductal tumor. (d) Micrograph of the specimen shows castlike tumor (stars) originating from and confined to mucosa filling the bile duct lumen. No tumor extends through the thickened fibromuscular layer of the duct wall (between arrows). L = liver parenchyma. (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (146K): [in this window] [in a new window] [Download PPT slide]   Figure 1d: Images in a 64-year-old man with well-differentiated tubular adenocarcinoma of the right intrahepatic duct confined to mucosa. (a) Subcostal transverse transabdominal US image of the liver shows a castlike intraductal mass in the upper part of right hepatic lobe. Note intact echogenic lines of the bile duct wall (arrows). (b, c) Transverse contrast-enhanced arterial phase CT images show intraductal mass filling bile ducts like a cast. Note intact wall of the bile ducts (arrow). Percutaneous transhepatic cholangiogram (not shown) demonstrated severe dilatation of anterior segmental ducts of the right hepatic lobe and obstruction by intraductal tumor. (d) Micrograph of the specimen shows castlike tumor (stars) originating from and confined to mucosa filling the bile duct lumen. No tumor extends through the thickened fibromuscular layer of the duct wall (between arrows). L = liver parenchyma. (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (165K): [in this window] [in a new window] [Download PPT slide]   Figure 2a: Images in a 64-year-old woman with papillary adenocarcinoma of intrahepatic and extrahepatic ducts. Tumor was confined to mucosa. (a) Oblique parasagittal transabdominal US image shows a fusiform intraluminal mass (arrows) filling the right hepatic duct, confluence, and upper part of the common hepatic duct. Note thin echogenic lines representing intact bile duct wall. GB = gallbladder. (b) Transverse arterial phase CT image shows an enhancing mass in right hepatic duct, but there is no demarcation between liver parenchyma and the mass (arrow). (c) Transverse CT image obtained 0.5 cm below b shows the mass in the common hepatic duct. Note the well-defined clear outer margin of the wall (arrow) without periductal fat infiltration. (d) Endoscopic retrograde cholangiogram shows an elongated filling defect representing intraductal tumor (arrow), but depth of wall invasion cannot be evaluated. (e) Micrograph of a section obtained through the right hepatic duct shows castlike papillary tumor filling the entire lumen. The tumor is confined to mucosa. Fibromuscular layer is thickened (area between arrows). (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (170K): [in this window] [in a new window] [Download PPT slide]   Figure 2b: Images in a 64-year-old woman with papillary adenocarcinoma of intrahepatic and extrahepatic ducts. Tumor was confined to mucosa. (a) Oblique parasagittal transabdominal US image shows a fusiform intraluminal mass (arrows) filling the right hepatic duct, confluence, and upper part of the common hepatic duct. Note thin echogenic lines representing intact bile duct wall. GB = gallbladder. (b) Transverse arterial phase CT image shows an enhancing mass in right hepatic duct, but there is no demarcation between liver parenchyma and the mass (arrow). (c) Transverse CT image obtained 0.5 cm below b shows the mass in the common hepatic duct. Note the well-defined clear outer margin of the wall (arrow) without periductal fat infiltration. (d) Endoscopic retrograde cholangiogram shows an elongated filling defect representing intraductal tumor (arrow), but depth of wall invasion cannot be evaluated. (e) Micrograph of a section obtained through the right hepatic duct shows castlike papillary tumor filling the entire lumen. The tumor is confined to mucosa. Fibromuscular layer is thickened (area between arrows). (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (168K): [in this window] [in a new window] [Download PPT slide]   Figure 2c: Images in a 64-year-old woman with papillary adenocarcinoma of intrahepatic and extrahepatic ducts. Tumor was confined to mucosa. (a) Oblique parasagittal transabdominal US image shows a fusiform intraluminal mass (arrows) filling the right hepatic duct, confluence, and upper part of the common hepatic duct. Note thin echogenic lines representing intact bile duct wall. GB = gallbladder. (b) Transverse arterial phase CT image shows an enhancing mass in right hepatic duct, but there is no demarcation between liver parenchyma and the mass (arrow). (c) Transverse CT image obtained 0.5 cm below b shows the mass in the common hepatic duct. Note the well-defined clear outer margin of the wall (arrow) without periductal fat infiltration. (d) Endoscopic retrograde cholangiogram shows an elongated filling defect representing intraductal tumor (arrow), but depth of wall invasion cannot be evaluated. (e) Micrograph of a section obtained through the right hepatic duct shows castlike papillary tumor filling the entire lumen. The tumor is confined to mucosa. Fibromuscular layer is thickened (area between arrows). (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (148K): [in this window] [in a new window] [Download PPT slide]   Figure 2d: Images in a 64-year-old woman with papillary adenocarcinoma of intrahepatic and extrahepatic ducts. Tumor was confined to mucosa. (a) Oblique parasagittal transabdominal US image shows a fusiform intraluminal mass (arrows) filling the right hepatic duct, confluence, and upper part of the common hepatic duct. Note thin echogenic lines representing intact bile duct wall. GB = gallbladder. (b) Transverse arterial phase CT image shows an enhancing mass in right hepatic duct, but there is no demarcation between liver parenchyma and the mass (arrow). (c) Transverse CT image obtained 0.5 cm below b shows the mass in the common hepatic duct. Note the well-defined clear outer margin of the wall (arrow) without periductal fat infiltration. (d) Endoscopic retrograde cholangiogram shows an elongated filling defect representing intraductal tumor (arrow), but depth of wall invasion cannot be evaluated. (e) Micrograph of a section obtained through the right hepatic duct shows castlike papillary tumor filling the entire lumen. The tumor is confined to mucosa. Fibromuscular layer is thickened (area between arrows). (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (132K): [in this window] [in a new window] [Download PPT slide]   Figure 2e: Images in a 64-year-old woman with papillary adenocarcinoma of intrahepatic and extrahepatic ducts. Tumor was confined to mucosa. (a) Oblique parasagittal transabdominal US image shows a fusiform intraluminal mass (arrows) filling the right hepatic duct, confluence, and upper part of the common hepatic duct. Note thin echogenic lines representing intact bile duct wall. GB = gallbladder. (b) Transverse arterial phase CT image shows an enhancing mass in right hepatic duct, but there is no demarcation between liver parenchyma and the mass (arrow). (c) Transverse CT image obtained 0.5 cm below b shows the mass in the common hepatic duct. Note the well-defined clear outer margin of the wall (arrow) without periductal fat infiltration. (d) Endoscopic retrograde cholangiogram shows an elongated filling defect representing intraductal tumor (arrow), but depth of wall invasion cannot be evaluated. (e) Micrograph of a section obtained through the right hepatic duct shows castlike papillary tumor filling the entire lumen. The tumor is confined to mucosa. Fibromuscular layer is thickened (area between arrows). (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (168K): [in this window] [in a new window] [Download PPT slide]   Figure 3a: Images in a 54-year-old man with papillary adenocarcinoma of the common bile duct confined to mucosa. (a) Oblique parasagittal transabdominal US image of extrahepatic bile duct shows an intraductal mass. Note intact thin echogenic lines (arrows) of the bile duct wall. (b) Transverse portal phase CT image shows an intraductal mass delineated by a thin enhancing wall (arrow) of the common bile duct. The attenuation of the mass was 40 HU on precontrast and 120 HU on postcontrast images. (c) Biliary drainage tube cholangiogram shows an intraluminal oval mass (arrows) with smooth margin. (d) Micrograph of the specimen shows papillary tumor confined to mucosa and attached to the thickened fibromuscular layer (arrows). Note normal thickness of the wall at the adjacent non–tumor-bearing duct (arrowhead). P = pancreas. (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (164K): [in this window] [in a new window] [Download PPT slide]   Figure 3b: Images in a 54-year-old man with papillary adenocarcinoma of the common bile duct confined to mucosa. (a) Oblique parasagittal transabdominal US image of extrahepatic bile duct shows an intraductal mass. Note intact thin echogenic lines (arrows) of the bile duct wall. (b) Transverse portal phase CT image shows an intraductal mass delineated by a thin enhancing wall (arrow) of the common bile duct. The attenuation of the mass was 40 HU on precontrast and 120 HU on postcontrast images. (c) Biliary drainage tube cholangiogram shows an intraluminal oval mass (arrows) with smooth margin. (d) Micrograph of the specimen shows papillary tumor confined to mucosa and attached to the thickened fibromuscular layer (arrows). Note normal thickness of the wall at the adjacent non–tumor-bearing duct (arrowhead). P = pancreas. (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (109K): [in this window] [in a new window] [Download PPT slide]   Figure 3c: Images in a 54-year-old man with papillary adenocarcinoma of the common bile duct confined to mucosa. (a) Oblique parasagittal transabdominal US image of extrahepatic bile duct shows an intraductal mass. Note intact thin echogenic lines (arrows) of the bile duct wall. (b) Transverse portal phase CT image shows an intraductal mass delineated by a thin enhancing wall (arrow) of the common bile duct. The attenuation of the mass was 40 HU on precontrast and 120 HU on postcontrast images. (c) Biliary drainage tube cholangiogram shows an intraluminal oval mass (arrows) with smooth margin. (d) Micrograph of the specimen shows papillary tumor confined to mucosa and attached to the thickened fibromuscular layer (arrows). Note normal thickness of the wall at the adjacent non–tumor-bearing duct (arrowhead). P = pancreas. (Hematoxylin-eosin stain; original magnification, x10.)

View larger version (136K): [in this window] [in a new window] [Download PPT slide]   Figure 3d: Images in a 54-year-old man with papillary adenocarcinoma of the common bile duct confined to mucosa. (a) Oblique parasagittal transabdominal US image of extrahepatic bile duct shows an intraductal mass. Note intact thin echogenic lines (arrows) of the bile duct wall. (b) Transverse portal phase CT image shows an intraductal mass delineated by a thin enhancing wall (arrow) of the common bile duct. The attenuation of the mass was 40 HU on precontrast and 120 HU on postcontrast images. (c) Biliary drainage tube cholangiogram shows an intraluminal oval mass (arrows) with smooth margin. (d) Micrograph of the specimen shows papillary tumor confined to mucosa and attached to the thickened fibromuscular layer (arrows). Note normal thickness of the wall at the adjacent non–tumor-bearing duct (arrowhead). P = pancreas. (Hematoxylin-eosin stain; original magnification, x10.)

Cholangiographic Features
Among the 18 cholangiograms, the size, shape, and extent of tumors were well demonstrated for 10 patients. The outer surfaces of tumor-bearing bile ducts were irregular because of the tumor itself (Fig 2), but it was not possible to evaluate whether the tumor involved the outer surface of the bile ducts or not. In six patients, only distal or proximal margins of the tumor were visualized because of complete bile duct obstruction by the tumor. In two patients, the tumor was not visualized because it was too small or was masked by mucin. In five patients, there was a large amount of intraductal mucin manifesting as ovoid, elongated, or amorphous filling defects, simulating intraductal tumors.

Bile ducts proximal to the tumor were dilated in all patients, depending on the degree of obstruction by the tumor. Ten patients showed complete obstruction and eight patients showed partial obstruction. In three patients, the entire biliary tree was dilated markedly because of excessive mucin, even though the bile duct was not completely obstructed because the mucin was thick and viscid and bile flow was impaired. The gallbladder was distended in three patients with carcinoma of the common bile duct.

MR Cholangiographic Features
In five patients, the tumor size and extent were well demonstrated on MR cholangiograms. In one patient, a small papillary intrahepatic tumor was depicted but an extrahepatic tumor was not depicted. In four patients with papillary carcinoma, the papillary surface of the tumor was well depicted. The dilated biliary tree was well demonstrated in all patients. It was not possible to evaluate the depth of tumor invasion or periductal infiltration.

Imaging-Pathologic Comparison
On the basis of the intact bile duct wall—that is, well-preserved echogenic lines of the tumor-bearing duct wall on US images and clear outer margin of the bile duct without periductal fat infiltration on CT images—four of 10 intrahepatic cholangiocarcinomas, four of five hilar cholangiocarcinomas, and all six extrahepatic cholangiocarcinomas could be diagnosed as an early bile duct carcinoma. However large and extensive the mass was, the bile duct wall remained intact and was visualized as smooth well-defined echogenic lines on US images and as a sharply defined outer margin or as a thin enhancing ring on CT images. There was no difference in image findings between early carcinoma confined to the mucosa and carcinoma that involved the fibromuscular layer of the bile duct wall. In the five patients in whom the bile duct wall was enhanced, the tumor-bearing fibromuscular layer of the duct was thickened up to 2.0 mm (Fig 3).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
In our study, US and CT demonstrations of the bile duct wall and its integrity were the most valuable findings for the evaluation of early bile duct carcinoma. At US, the bile duct wall is more echogenic than the tumor mass because of the periductal fat. Because of the fibrofatty tissue of the perimuscular layer, the intrahepatic and extrahepatic bile duct wall was delineated as clear, thin, echogenic lines on longitudinal scans and as rings on transverse scans. On CT images, the wall of the normal extrahepatic duct is delineated as a thin ring. The wall of the normal intrahepatic bile ducts is not delineated on CT images because there is scanty fat around the intrahepatic bile ducts. In our patients with early bile duct carcinoma, the tumor-bearing bile ducts were clearly delineated as a sharply defined outer margin or as a thin enhancing ring, sometimes more densely enhanced than the tumor mass. A thickened fibromuscular layer of the tumor-bearing bile duct wall seems to be responsible. The periductal fat was clear and not infiltrated.

In some patients with early bile duct carcinoma, the tumor was large and fairly extensive, involving both intrahepatic and extrahepatic ducts. This is probably because tumor cells grow and spread superficially along the bile duct mucosa and do not invade deeply into the fibromuscular layer (10–14). Even in the patients in whom the tumor mass was large and extensive, ductal wall integrity was preserved and there was no evidence of periductal infiltration on US or CT images.

However, there are limitations to the imaging diagnosis of early bile duct carcinoma. It is not always possible to depict the distal part of the common bile duct at US because of duodenal or colon gas. On CT images, it is difficult to determine whether the bile duct wall or periductal tissue has been infiltrated because of partial volume averaging with adjacent organs, such as the pancreas, or because of scanty fat around the bile ducts. It is difficult to determine periductal tumor infiltration in intrahepatic bile duct tumors because there is little periductal fat in the portal triads. In this regard, US is better for the determination of periductal tumor infiltration because the periductal fat can be delineated as echogenic. With US or CT, it is not possible to distinguish between invasion of the mucosa from invasion of the fibromuscular layer. Although cholangiography and MR cholangiography allow the size, shape, and extent of a tumor to be precisely evaluated, it is not possible to determine the depth of tumor invasion in the bile duct wall. When a tumor mass is small and located at the confluence or branching area of the intrahepatic bile ducts, the mass cannot be depicted because of the complex anatomy of the bile ducts; therefore, it is not possible to correctly stage the tumor, as in two of our patients. Endoscopic US of the bile ducts is increasingly being used because the resolution of endoscopic US is better than that of transabdominal US. Thus, a small tumor can be detected and the depth of tumor invasion can be better evaluated (9). In this regard, endoscopic biliary US certainly offers an improved means for the diagnosis and staging of early bile duct carcinoma (15–17).

The radiologic diagnosis of early bile duct carcinoma is important because if the tumor is resected, the prognosis is excellent. For patients with carcinoma infiltrating beyond the bile duct, such as a mass-forming and periductal-infiltrating cholangiocarcinoma, prognosis is poor even with extensive radical surgery (18–21). Authors have reported a 5-year survival rate of 27% in patients who underwent radical surgery (22). In contrast, for patients with carcinoma limited to the bile ducts, tumor resection with a tumor-free margin offers long-term survival.

There ware several limitations to our study. With regard to the relationship between the anatomic structure of the bile duct and the corresponding imaging findings, it is generally believed that hyperechoic lines on transabdominal US images match the complex interface of the fluid and the mucosa and the three anatomic structures: the mucosa, the fibromuscular layer, and the subserosal fat tissue. Thus, histologic layers of the bile duct cannot be differentiated at transabdominal US. On CT images, an enhanced thin tube or ring corresponds to the mucosa and the fibromuscular layer. Therefore, it may be difficult to differentiate early bile duct carcinoma limited to the mucosa and fibromuscular layer from advanced carcinoma invading the perimuscular fat layer. Tamada et al (9) reported that intraductal US allowed differentiation of early bile duct carcinoma limited to the mucosa and fibromuscular layer from carcinoma extended to the perimuscular connective tissue in 77% of cases. This was an intrinsic weakness of our study, and further study that includes cases of advanced bile duct carcinoma is necessary. There were other limitations, including the retrospective nature of the study; the fact that radiologists knew the diagnosis of early bile duct carcinoma when they reviewed the images; unknown sensitivity and specificity of the imaging features because of the relatively small sample size, which included only patients with early bile duct cancer; and the heterogeneity of imaging methods over a long period, including varying section thicknesses at CT scanning. Because the images were reviewed with consensus reading, it was not possible to evaluate individual radiologic findings and interobserver variability.

In conclusion, early bile duct carcinoma appears as an intraductal mass with preservation of the bile duct wall integrity with a clear outer margin, regardless of the size or extent of the tumor.

	ACKNOWLEDGMENTS

 
The authors thank Chan Sup Shim, MD, Digestive Disease Center, Soon Chun Hyang Hospital, for his invaluable comments on the management of bile duct cancer; John Roberts, PhD, Harrisco, for his copyediting; and Young Joo Moon, Samsung Medical Center, for her help in manuscript preparation.

	FOOTNOTES

 
Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, J.H.L.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, J.H.L.; clinical studies, all authors; statistical analysis, J.H.L., K.T.J.; and manuscript editing, J.H.L.

	References

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 

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