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DOI:10.2214/AJR.05.0008
AJR 2006; 186:1580-1586
© American Roentgen Ray Society


Clinical Observations

Preoperative Evaluation of Resectability of Klatskin Tumor with 16-MDCT Angiography and Cholangiography

H. W. Chen1, A. Z. Pan1, Z. J. Zhen1, S. Y. Su1, J. H. Wang1, S. C. H. Yu2 and W. Y. Lau2

1 Department of Hepatobiliary Surgery, The First People's Hospital of Fo Shan, Fo Shan 528000, Guang Dong, People's Republic of China.
2 Department of Surgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, People's Republic of China.

Received January 4, 2005; accepted after revision July 7, 2005.

 
Address correspondence to H. W. Chen (chwei{at}fsyyy.com).


Abstract
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. The objective of our study was to evaluate prospectively the preoperative use of 16-MDCT angiography and cholangiography in determining the resectability of Klatskin tumors.

CONCLUSION. Preoperative MDCT angiography and cholangiography gave a good assessment of the degree of vascular and biliary involvement of the Klatskin tumor.

Keywords: biliary cholangiocarcinoma • cholangiography • Klatskin tumor • MDCT angiography


Introduction
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
In recent years, with the invention and development of the technology of MDCT, increasing numbers of reports have been published on its use for preoperative assessment of liver tumors and pancreatic tumors [1, 2]. But few reports of its use for the preoperative assessment of Klatskin tumors are available. We conducted a prospective study on the use of 16-MDCT angiography and cholangiography in the preoperative assessment of the resectability of Klatskin tumors, with the goal of evaluating its accuracy and clinical value.


Subjects and Methods
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
General Information
From January 2002 to June 2004, 18 patients with Klatskin tumors were recruited for preoperative assessment with MDCT angiography and cholangiography. The diagnosis of Klatskin tumor was subsequently confirmed in all 18 patients with histologic examination of the surgically resected or biopsy specimens.

Thirteen men and five women participated in the study, with an average age of 60.6 years and an age range of 38 to 73 years. The major presenting symptom was painless progressive jaundice occurring for 1 week to 1 month, with a mean of 15 days. The tumors were detected with sonography or MR cholangiopancreatogram. All patients underwent laparotomy 10 to 14 days after CT examination. Tumor resection was performed in four patients. Resection of the right hemiliver and caudate lobe was performed in six patients. Resection of the left hemiliver and caudate lobe was performed in two patients. Palliative internal drainage was performed in two patients. U-tube external drainage was performed in three patients; metallic biliary stenting was performed in one patient.

Equipment
The equipment used was a 16-MDCT unit; imaging was performed with tube voltage, 120 kV; tube current, 250 mA; scanning time, 0.5 sec; slice thickness, 2.5 mm; volumetric reconstruction interval, 1.25 mm; pitch, 1.375; and detector group thickness, 1.25 mm.

Study Method
All patients underwent standard and sonographically guided percutaneous transhepatic biliary drainage before surgery. An 8.5-French pigtail catheter was used in all patients. Unilateral drainage was performed in four patients. Bilateral drainage was performed in 14 patients. The catheters were placed at the intrahepatic bile ducts for external biliary drainage. The CT examination was performed first, with a plain scan of the liver, followed by a triphasic contrast-enhanced CT at 25 sec, 45 sec, and 65 sec after an injection of 120 mL of nonionic contrast medium (300 mg I/mL) given at the antecubital vein at a rate of 3 mL/sec, to catch the early arterial phase, late arterial-early portal venous phase, and hepatic venous phase, respectively. The liver was scanned again when 30-40 mL of 10% meglumine iothalamate (Conray, Mallinckrodt) was instilled into the biliary tree through the pigtail catheter at 5 min after the triphasic CT, with the patients holding their breath.

The data acquired were transferred to a workstation (Advantage Windows 4.1, GE Healthcare) for reconstruction of the 3D images of the portal venous system, hepatic arteries, and the biliary tree. The data were processed with the techniques of volumetric reconstruction, multiplanar reconstruction, and maximum intensity projection. Tumor resectability was assessed according to the following criteria: the site and type of biliary obstruction, the relationship of the tumor and blood vessels at the porta hepatis, evidence of tumor infiltration of the second-order branch of the bilateral hepatic ducts, evidence of tumor involvement of the proper hepatic artery together with the left or right hepatic artery, evidence of involvement of both the right and left branches of the portal vein, and evidence of distal metastasis or retroperitoneal lymph node metastasis. The criteria used for diagnosing tumor invasion of blood vessels or bile ducts was the detection of irregularity of the endoluminal surface of the structure, straightening of the structure, narrowing of the structure, or occlusion of the structure. The CT images were interpreted by the consensus of three radiologists experienced in hepatobiliary CT. The results of preoperative assessment of tumor resectability were compared with the results of assessment at laparotomy. Statistical analysis was performed with the kappa test.


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Table 1 shows the CT and operative findings of all 18 patients.


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TABLE 1: CT and Intraoperative Findings

 

Relationship of the Tumor to the Hepatic Artery and Portal Vein at the Porta Hepatis
Portal vein invasion was detected on MDCT angiography in 13 patients, and these were all confirmed at laparotomy. Of the five patients in whom no portal vein invasion was detected on MDCT angiography, four patients were confirmed at laparotomy to have no portal vein invasion; one patient was confirmed to have portal vein invasion. The diagnostic accuracy was 94.4% (17/18; 95% confidence interval [CI], 72.7-99.9%). Hepatic artery invasion was detected on MDCT angiography in 11 patients; all of these were confirmed at laparotomy. Of the seven patients in whom no hepatic artery invasion was detected on MDCT angiography, five patients were confirmed at laparotomy to have no hepatic artery invasion; two patients were confirmed to have hepatic artery invasion. The diagnostic accuracy was 88.9% (16/18; 95% CI, 65.3-98.6%).

Site and Type of Biliary Obstruction
The preoperative CT cholangiography showed that biliary obstruction had occurred at the porta hepatis in all patients. Based on the Bismuth classification (1975) [3] of biliary obstruction, two patients had type I obstruction; two patients, type II obstruction; four patients, type IIIa obstruction; two patients, type IIIb obstruction; and eight patients, type IV obstruction. The operative findings of the site and type of biliary obstruction were the same as the CT findings in all patients. Diagnostic accuracy was 100% (95% CI, 81.5-100%).

Preoperative Assessment of the Resectability of Klatskin Tumor with CT
The tumors in 12 patients were considered resectable in the preoperative assessment with CT. Of these, 11 tumors were actually resectable; therefore, the accuracy of CT assessment of resectability was 91.7% (11/12; 95% CI, 61.5-99.8%). Of the six tumors considered to be unresectable with preoperative CT, five were actually unresectable, and the other tumor became resectable after the main portal vein was partially resected; therefore, the accuracy of CT assessment of unresectability was 83.3% (5/6; 95% CI, 35.9-99.6%). When the results of preoperative CT assessment of tumor resectability were compared with the results of intraoperative assessment, which was used as the gold standard, statistical analysis with the kappa test showed a kappa value of 0.784 ({kappa} >0), indicating that preoperative CT assessment had a good correlation with the intraoperative assessment.


Discussion
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
The resectability of Klatskin tumors is determined by the following factors: first, whether the second-order branch of the bilateral hepatic ducts has been infiltrated by the tumor; second, whether the proper hepatic artery has become involved together with the left or right hepatic arteries; and third, whether the second-order branches of the main portal vein have become involved simultaneously. If tumor resectability is accurately assessed preoperatively, unnecessary operation can be avoided, and the relatively less invasive nonoperative treatment options such as endoscopic or percutaneous placement of biliary endoprostheses can be adopted [4]. A direct and comprehensive technique of clinical investigation for the preoperative assessment of resectability of Klatskin tumor currently is still lacking. Liang et al. [5] reported the use of color Doppler sonography in the preoperative assessment of the relationship between tumors and blood vessels at the porta hepatis. The diagnostic accuracy for the relationship between tumor and portal vein was 81.82%, and the diagnostic accuracy for the relationship between tumor and portal vein was 77.27%, indicating that color Doppler sonography is valuable for the preoperative assessment of the resectability of Klatskin tumors [5]. In the last few years, MR cholangiopancreatography (MRCP) has become a rapidly developing technology for the noninvasive imaging of the pancreatic and biliary ductal system, replacing endoscopic retrograde cholangiopancreatography (ERCP) and percutaneous transhepatic cholangiography (PTC) as the first-line investigatory method for biliary obstruction [6, 7]. The diagnostic accuracy of MRCP in locating the site of biliary obstruction and in showing the cause of biliary obstruction was 100% and 95%, respectively [8]. Selective angiography is uncommonly performed today because it is an invasive procedure requiring arterial catheterization with a risk of complications, and it only provides an indirect portovenogram. Although each of the investigatory techniques just described carries its own merits, they can only evaluate the condition of an isolated vascular or biliary system; they cannot provide information on the relationship among the tumor, important vessels, and bile ducts at the porta hepatis. Therefore, a proper assessment of tumor resectability requires a combination of the results of several different investigations.

MDCT angiography is a vascular imaging technology that involves the continuous volumetric acquisition of anatomic, pathologic, and physiologic data by an MDCT scanner at the peak arterial phase of contrast enhancement, computerized postacquisition data processing, and ultimately reconstruction of a 3D image of the target vessels. The introduction of MDCT angiography not only significantly increases the accuracy of the diagnosis and localization of Klatskin tumor, it also provides a unique advantage in preoperative tumor staging and assessment of tumor resectability by 3D vascular imaging [9, 10].

Two major clinical applications of MDCT angiography have proved valuable.

Precise Demonstration of the Relationship of the Tumor, Hepatic Artery, and Portal Vein with 3D Reconstruction of CT Angiography
In the present series, the diagnostic accuracy of MDCT angiography in the preoperative assessment of the relationship between tumor and portal vein was 94.4%, and the diagnostic accuracy in the assessment of the relationship between tumor and hepatic artery was 88.9%. These results were superior to those of color Doppler sonography [5]. In patient 1 of the present series, MDCT angiography showed obvious evidence of tumor invasion of the right and left branches of the portal vein and the right hepatic artery that were of reduced caliber and narrowed, whereas the left hepatic artery was intact (Figs. 1B and 1C). At laparotomy, tumor invasion of the right hepatic artery, the right and left branches of the portal vein, and portal vein bifurcation was confirmed. Right hemihepatectomy and resection of the tumor-involved portal bifurcation were performed, followed by end-to-end anastomosis of the left branch and the main trunk of the portal vein. In patient 2, MDCT angiography showed that the right branch of the portal vein and the right hepatic artery were uninvolved by the tumor; however, the peripheral end of the left branch of the portal vein and the left hepatic artery were irregularly narrowed with reduced caliber (Figs. 2B and 2C). At laparotomy, these findings were confirmed. Moreover, tumor invasion of the left hepatic duct and caudate lobe bile duct was also noted (Fig. 2A). Left hemihepatectomy and resection of the caudate lobe were therefore performed. In patient 3, MDCT angiography showed obvious narrowing of the left branch of the portal vein, irregularity of the anterior wall of the right branch of the portal vein, together with narrowing and reduced caliber of the bilateral hepatic arteries, indicating tumor invasion of all these structures (Figs. 3B and 3C). At laparotomy, tumor invasion of the left and right branches of the portal vein and the left and right hepatic arteries was found. The tumor was unresectable. A U-tube was then placed for biliary drainage. U-tube drainage is a surgical intubation procedure indicated for those patients with unresectable tumors found at laparotomy. The tube, consisting of a transhepatic upper limb and a subhepatic lower limb extending out of the patient's body surface and connected to each other in a U-shaped close loop, provides a large-bore channel for palliative drainage of the obstructed ducts [11, 12].


Figure 2
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Fig. 1B —Preoperative 3D reconstructed CT angiography and cholangiography of 73-year-old man. Reconstructed hepatic arteriogram showed evidence of invasion of right hepatic artery (RHA) with reduced caliber and narrowed lumen.

 

Figure 3
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Fig. 1C —Preoperative 3D reconstructed CT angiography and cholangiography of 73-year-old man. Reconstructed portovenogram showed tumor located superior to portal bifurcation. Evidence of tumor invasion of right branch of portal vein (right portal vein [RPV]) was noted, with truncation and disappearance of its peripheral end. Tumor invasion was also noted at anterior wall of origin of left branch of portal vein (left portal vein [LPV]). This finding was confirmed at surgery.

 

Figure 5
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Fig. 2B —Preoperative 3D reconstructed CT angiography and cholangiography of 69-year-old man. Reconstructed hepatic arteriogram showed normal proper hepatic artery and right hepatic artery (RHA) (arrow). Peripheral segment of left hepatic artery (LHA) was of reduced caliber and narrowed (arrow).

 

Figure 6
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Fig. 2C —Preoperative 3D reconstructed CT angiography and cholangiography of 69-year-old man. Reconstructed portovenogram showed normal main trunk and right branch of portal vein (RPV) (arrow). Peripheral end of left branch of portal vein was irregularly narrowed (LPV) (arrow).

 

Figure 4
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Fig. 2A —Preoperative 3D reconstructed CT angiography and cholangiography of 69-year-old man. Catheter cholangiogram of right biliary ductal system showed evidence of dilatation of right intrahepatic bile ducts. There was contrast filling defect at confluence of right and left hepatic ducts and common hepatic duct (arrow). Filling defect was more obvious on left side. Left hepatic duct was not outlined with contrast agent but common hepatic duct was outlined, indicating porta hepatis tumor was located at junction between common hepatic duct and left hepatic duct.

 

Figure 8
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Fig. 3B —Preoperative 3D reconstructed CT angiography and cholangiography of 38-year-old woman. Reconstructed hepatic arteriogram showed tumor invasion of left (LHA) and right (RHA) hepatic arteries that were of reduced caliber and narrowed (arrows).

 

Figure 9
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Fig. 3C —Preoperative 3D reconstructed CT angiography and cholangiography of 38-year-old woman. Reconstructed portovenogram showed evidence of tumor encasement and occlusion of left branch of portal vein (LPV) (arrow) and tumor invasion of anterior wall of right branch of portal vein (RPV), with mild surface irregularity (arrow).

 


Figure 1
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Fig. 1A —Preoperative 3D reconstructed CT angiography and cholangiography of 73-year-old man. Catheter cholangiogram of bilateral system performed with percutaneous transhepatic biliary drainage catheter showed moderate dilatation of left (LHD) and right (RHD) hepatic ducts. Underfilling was noted at confluence of intrahepatic ducts and common bile duct (CBD). RHD was more obviously affected and probably completely occluded. Obvious narrowing of LHD was noted at confluence, although contrast agent could still pass into common hepatic duct.

 


Figure 7
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Fig. 3A —Preoperative 3D reconstructed CT angiography and cholangiography of 38-year-old woman. Catheter cholangiogram with pigtail catheters placed within bilateral system showed dilatation of left (LHD) and right (RHD) hepatic bile ducts, with left ducts more severely affected. There was underfilling at confluence of LHD and RHD and common bile duct (CBD). Tumor invasion was noted in right and left hepatic ducts (arrows), although contrast agent can still partially pass into common hepatic duct. GB = gallbladder.

 


Figure 10
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Fig. 4A —Cholangiograms of 80-year-old man. Preoperative CT cholangiogram showed stenosis of common hepatic duct (CHD) and proximal segment of posterior right hepatic duct (PRHD), signifying tumor invasion at these sites and Bismuth classification IIIa. ARHD = anterior right hepatic duct; CBD = common bile duct; GB = gallbladder.

 


Figure 11
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Fig. 4B —Cholangiograms of 80-year-old man. MR cholangiogram only showed stenosis of CBD: Bismuth classification II (arrow).

 


Figure 12
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Fig. 4C —Cholangiograms of 80-year-old man. Percutaneous transhepatic cholangiogram only showed filling defect at CBD: Bismuth classification II (arrow).

 
Precise Demonstration of the Site and Extent of Biliary Obstruction by CT Catheter Cholangiogram and 3D Reconstruction of the Biliary Tree
Three-dimensional biliary tree imaging allows accurate preoperative Bismuth staging and provides important information for planning the approach to biliary drainage. In the present series, the accuracy of preoperative staging was 100%. The authors found that CT cholangiograms have the advantages of high spatial resolution, precise visualization of anatomic structures, and multidirectional assessment of biliary branches, and therefore they provide important information for localization and staging of the tumor (Figs. 4A, 4B and4C). In patient 1, CT cholangiogram clearly showed that the biliary tumor at the porta hepatis was located at the right hepatic duct and common hepatic duct, with the origin of the second-order branch of the left hepatic duct uninvolved (Fig. 1A). Based on this information, a right hemihepatectomy was planned preoperatively to preserve the left hemiliver. The preoperative findings were confirmed intraoperatively.

In patient 2, CT cholangiogram showed that the tumor at the porta hepatis was mainly located at the left hepatic duct and common hepatic duct, with the origin of the second-order branch of the right hepatic duct uninvolved. Left hemihepatectomy was planned preoperatively. The findings were confirmed at laparotomy.

The proportion of circumferential contact of the tumor with a blood vessel or bile duct is important information and should have been included in the diagnostic criteria of tumor invasion. It was found retrospectively that neglecting circumferential contact by the tumor was a major cause of error leading to the underdiagnosis of tumor invasion, and the structure is most probably invaded if it is surrounded by tumor for half or more of its circumference.

In conclusion, 3D MDCT angiography and cholangiography are useful diagnostic tools for delineation of the relationship between the tumor and the important vessels at the porta hepatis and for tumor staging. They therefore provide important information on the preoperative assessment of tumor resectability and the extent of surgery. It is believed that this investigatory technique shows the relationship of the tumor, blood vessels, and bile ducts with a higher definition and a more direct and comprehensive perspective when compared with the other currently available investigatory methods and therefore deserves a wider clinical application.


References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

  1. Ling H, Guan Y, Ding B, Lin X, Zhang H, Chen K. Vascular involvement in pancreatic carcinoma: preoperative assessment by multislice CT angiography. Clin J Radiol 2002;36 : 609-612
  2. Wigmore SJ, Redhead DN, Yan XJ, et al. Virtual hepatic resection using three dimensional reconstruction of helical computed tomography angioportograms. Ann Surg 2001;233 : 221-226[CrossRef][Medline]
  3. Bismuth H, Corlette MB. Intrahepatic cholangioenteric anastomosis in carcinoma of the hilus of the liver. Surg Gynecol Obstet 1975; 140:170 -178[Medline]
  4. Nimura Y, Kamiya J, Kondo S, et al. Aggressive preoperative management and extended surgery for hilar cholangiocarcinoma: Nagoya experience. J Hepatobiliary Pancreat Surg2000; 7:155 -162[CrossRef][Medline]
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  7. Vaishali MD, Agarwal AK, Upadhyaya DN, et al. Magnetic resonance cholangiopancreatography in obstructive jaundice. J Clin Gastroenterol 2004; 38:887 -890[Medline]
  8. Zhou JX, Liang BL, Xu LY, Huang SQ. MR cholangiopancreatography and MR imaging in the diagnosis of extrahepatic cholangiocarcinoma. Clin J Oncol 2004;26 : 421-423
  9. Tillich M, Mischiroger HJ. Preisegger KH, et al. Multiphasic helical CT in diagnosis and staging of hilar cholangiocarcinoma. AJR 1998; 171:651 -658[Abstract/Free Full Text]
  10. Cha JH, Han JK, Kim TK. Preoperative evaluation of Klatskin tumor: accuracy of spiral CT in determining vascular invasion as a sign of unresectability. Abdom Imaging 2000;25 : 500-507[CrossRef][Medline]
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  12. Krige JEJ, Terblanche J. Dilatation and transhepatic intubation: the U tube. In: Terblanche J, ed. Hepatobiliary malignancy: its multidisciplinary management. London, UK: Edward Arnold,1994

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