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by the American Institute of Ultrasound in Medicine J Ultrasound Med 21:767-772 • 0278-4297 Color Doppler Sonography of Bile Duct Tumor Thrombi in Hepatocellular CarcinomaDivision of Hepatogastroenterology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan, Republic of China. Address correspondence and reprint requests to Sheng-Nan Lu, MD, PhD, Division of Hepatogastroenterology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, 123 Ta-Pei Rd, Niaosung 833, Kaohsiung, Taiwan, Republic of China.
Objective. To determine with the use of color Doppler sonography whether bile duct tumor thrombi had detectable vasculature in hepatocellular carcinoma. Methods. Among 491 patients with tissue-proven hepatocellular carcinoma, 9 (1.8%) had bile duct tumor thrombi. All 9 patients had spectral Doppler sonography guided by color Doppler sonography (3.75-MHz convex probe). Results. All 9 patients had dilated bile ducts with isoechoic thrombi. Eight patients had tumors infiltrating into and obstructing adjacent major bile ducts. The other patient had common hepatic duct tumor emboli that were not adjacent to primary tumors. Color signals were detectable within bile duct tumor thrombi in 7 patients. All of them had pulsatile waveforms on spectral analyses. Conclusions. Bile duct tumor thrombosis with obstructive jaundice was a rare complication of hepatocellular carcinoma. A detectable color signal with pulsatile waveforms was shown in most cases by color Doppler sonography with spectral analyses.
Key Words: bile duct tumor thrombi • color Doppler sonography • hepatocellular carcinoma Abbreviations: CDS, color Doppler sonography • ERC, endoscopic retrograde cholangiography • HCC, hepatocellular carcinoma • MR, magnetic resonance • PTC, percutaneous transhepatic cholangiography
Hepatocellular carcinoma (HCC) is one of the most common malignant tumors in the world.1 Jaundice has been reported in up to 40% of cases, mostly attributable to underlying cirrhosis or extensive tumor infiltration.2,3 Intrahepatic bile duct dilatation secondary to HCC was a rare cause of jaundice. It had been attributed to tumor compression, tumor emboli with hemobilia, or tumor infiltrating into and obstructing major bile ducts, resulting in obstructive jaundice.4 Conventional imaging modalities, including sonography, computed tomography, magnetic resonance (MR) imaging, endoscopic retrograde cholangiography (ERC), and percutaneous transhepatic cholangiography (PTC), were useful in the diagnosis of the various causes of obstructive jaundice, but their usefulness in characterization of bile duct thrombi was limited. Color Doppler sonography (CDS) is a noninvasive method in liver hemodynamic studies. Because HCC is known to be a hypervascular tumor, CDS is useful in detection of blood flow in HCC and helpful in differentiating it from other liver tumors.5 Arterial blood flow in bile duct HCC was shown on CDS in a prior case report.6 Here we report the results in a larger series of patients.
There were 491 patients with tissue-proven HCC admitted to this department between September 1998 and October 2000. We reviewed the clinical records and reports of computed tomography and sonography in all patients. Nine patients with bile duct thrombi were identified and were included in this study. All 9 patients had liver tumors and bile duct thrombi, the characteristics of which were not known. Bile duct thrombi were confirmed to be HCC by fine-needle aspiration (Chiba needle, 22 gauge, 150 mm) from the thrombi. The patients were 6 men and 3 women ranging in age from 27 to 75 years (mean ± SD, 52.8 ± 14.4 years). All patients had liver cirrhosis. Liver function reserve was Child class A in 5 patients, class B in 3 patients, and class C in the other patient. Eight patients had hepatitis B virus surface antigen, and the other patient had hepatitis C virus antibody. Total bilirubin levels ranged from 0.8 to 16.2 mg/dL (mean ± SD, 5.3 ± 5.6 mg/dL). Multifocal HCCs were detected on imaging studies in 5 patients, and solitary HCCs were detected in the other 4 patients. The largest tumor size measured with sonography ranged from 2.5 to 19 cm (mean ± SD, 7.5 ± 6.0 cm). Bile duct thrombi were shown on sonography and computed tomography in all patients. Four patients had ERC; 1 had PTC; and 1 had MR cholangiography. Color Doppler sonography was applied to bile duct tumor thrombi to show the blood flow within the thrombi. All CDS studies were performed by 1 author (J.-H.W.) using a 3.75-MHz convex probe combined with a color Doppler system (340A; Toshiba Medical Systems Co, Ltd, Tokyo, Japan). The optimal conditions of color and spectral imaging were set dynamically during examination to provide a clear image, to prevent aliasing, and to minimize background interference. The performer set optimization of the color Doppler technique subjectively. All patients were examined during suspended respiration in the supine position without overnight fasting. Color Doppler sonography was used to find the regions of color signal, and the vasculature was definitely determined by spectral Doppler sonography. The Doppler cursor was manipulated under CDS imaging guidance within the thrombus to detect the waveform and the direction of the flow. The sample width was set to encompass the color signal with care taken not to exceed the margin of thrombus.
Bile duct tumor thrombi were detected in 9 (1.8%) of 491 patients. Hepatocellular carcinoma with infiltration into and obstruction of adjacent bile ducts was shown in 8 patients. Common hepatic duct tumor thrombi not adjacent to primary tumors, which were defined as bile duct tumor emboli, were shown in the other patient. Two patients had coexisting portal main trunk thrombosis. All 9 patients had dilated bile ducts with isoechoic thrombi. Tumor thrombi within the right hepatic duct extending to the common hepatic duct were shown in 4 patients, and thrombi within the left hepatic duct extending to the common hepatic duct were shown in 1 patient. Two patients had left hepatic duct thrombi, and 1 patient had right hepatic duct thrombi. The other patient had common hepatic duct emboli.
Color signals were detected from bile duct thrombi in 7 patients. Pulsatile waveforms were shown on spectral analysis in all 7 patients (Figs. 1 and 2
Obstructive jaundice with intrahepatic duct dilatation has been regarded as a rare complication of HCC. It has been reported in 3.3% of HCC cases.7 Icteric-type HCC with bile duct invasion by tumor was reported in 0.7% to 3.6% of cases in various imaging studies.7–9 It has been reported in 2.5% to 9.5% of surgical cases and in 9.2% of autopsy cases.10,11 Tumor emboli with obstruction were reported in 17.6% of cases in a surgical series.10 Because bile duct invasion by tumor is an advanced stage of HCC, portal vein invasion has been frequent and has been reported in 78% to 88% of patients.7,11 In our series, the prevalence of bile duct thrombi (1.8%) was similar to that of other reports, whereas the prevalence of coexisting portal vein thrombosis (22.2%) was less than in previous studies. Tumor emboli were shown in only 1 patient (11%). Because sonography is less sensitive than surgery in detecting tumor invasion, it might explain the lower detection rate in our series. Bile duct thrombi might be benign, malignant, or a combination of both. Benign thrombi could be blood clots, pus, or sludge. Malignant thrombi could be primary intrabiliary malignant tumors, HCC with invasion to bile ducts, or metastatic cancer with bile duct invasion. It is important to characterize bile duct thrombi to determine the therapeutic strategy and prognosis. It has been shown that hepatic resection and removal of bile duct thrombi without bile duct resection has been a successful treatment in patients with HCC and bile duct thrombi.10,12 A combination of biliary drainage and transcatheter arterial embolization also has been recommended as a preoperative strategy.8 Endoscopic retrograde cholangiography and PTC are useful in the diagnosis of intrabiliary thrombi. Intraductal filling defects resulting in partial or complete obstruction and ductal dilatation were shown in 70% of bile duct invasion by HCC, but the cholangiographic features were not diagnostic for bile duct invasion by HCC13; therefore, ERC and PTC are limited in their usefulness for characterization of bile duct thrombi. The MR features of intraductal tumors, bile duct obstruction with an associated hepatic mass or localized intrahepatic duct dilatation within wedge-shaped areas, indicated intraductal tumor extension.14,15 The enhancement of intraductal masses on dynamic MR images showed an extension of HCC rather than blood clots.14 Magnetic resonance cholangiography was recently shown to be superior to ERCP in detecting the presence of biliary obstruction, but it was relatively ineffective for interpretation of icteric-type HCC.16 For detection of tumor vascularity, spectral Doppler sonography guided by CDS was shown to be useful in the differential diagnosis of liver tumors.17 It was also useful in detection of blood flow within portal vein thrombosis in liver cirrhosis. Reports have shown that it is a useful method for differentiating malignant from benign portal vein thrombi in liver cirrhosis, with 45% to 90% sensitivity and 95% to 100% specificity.18 The usefulness of CDS in characterization of bile duct tumor thrombi in HCC, however, had not been evaluated. The mechanism of obstructive jaundice–associated bile duct tumor thrombi was considered to be HCC growing into the bile duct, incarceration of a part of HCC, or a clot. In our series, CDS showed blood flow in bile duct tumor thrombi in 7 (87.5%) of 8 patients with HCC and bile duct infiltration. Pulsatile flow was shown on spectral analysis in all 7 patients. Power Doppler sonography, a technique based on the integrated power of the Doppler spectrum, is more sensitive than CDS in depicting vascular flow in HCC. Its utility in detection of vascularity of bile duct tumor thrombi in patients with HCC might be more sensitive than that of CDS. Further study is needed. In conclusion, bile duct tumor thrombi in patients with HCC were rare complications. Color Doppler sonography was sensitive for detection of the vascularity of bile duct tumor thrombi in these patients. It was useful in characterization and might be helpful in the differential diagnosis of bile duct thrombi.
Received January 24, 2002, from the Division of Hepatogastroenterology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan, Republic of China.
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Abstract
Introduction
