DOI:10.2214/AJR.07.3992
AJR 2008; 191:1448-1457
© American Roentgen Ray Society
Hilar Cholangiocarcinoma: Role of Preoperative Imaging with Sonography, MDCT, MRI, and Direct Cholangiography
Jin-Young Choi1,
Myeong-Jin Kim1,
Jeong Min Lee2,
Ki Whang Kim1,
Jae Young Lee2,
Joon Koo Han2 and
Byung Ihn Choi2
1 Department of Radiology, Research Institute of Radiological Science, Institute
of Gastroenterology, Yonsei University Health System, Seodaemun-ku
Shinchon-dong 134, Seoul, 120-752, Republic of Korea.
2 Department of Radiology, Seoul National University Hospital, Seoul, Republic
of Korea.
Received March 15, 2008;
accepted after revision May 21, 2008.
Address correspondence to M. J. Kim
(kimnex{at}yuhs.ac).
Abstract
OBJECTIVE. The purpose of this article is to describe the roles of
sonography, MDCT, MRI, and direct cholangiography in the evaluation of hilar
cholangiocarcinoma.
CONCLUSION. Hilar cholangiocarcinoma is a primary malignant tumor
typically located at the confluence of the right and left ducts within the
porta hepatis. Staging of hilar cholangiocarcinoma with various imaging
techniques is crucial for management, and a comprehensive approach is needed
for accurate preoperative assessment.
Keywords: cholangiography • CT • hilar cholangiocarcinoma • MRI • sonography
Introduction
Cholangiocarcinoma is classified as intrahepatic, hilar, or extrahepatic
[1,
2]. Approximately 60–70%
of the tumors originate at the bifurcation of the hepatic ducts, and
20–30% originate in the distal common bile duct
[3]. Hilar cholangiocarcinoma,
or Klatskin's tumor, is a tumor originating in the confluence of the right and
left ducts within the porta hepatis
[4]. This tumor has been
erroneously classified as intrahepatic in some epidemiologic studies, but it
should be classified as extrahepatic in terms of anatomic location or in a
separate category based on the topographic site of origin
[1–3,
5,
6].
Surgical resection is the only effective curative therapy for hilar
cholangiocarcinoma. Unfortunately, fewer than one half of patients are
candidates for curative resection because of the tendency of the tumor to
spread by direct extension into adjacent organs and tissues, including the
large portal veins and hepatic arteries
[7,
8]. Therefore, imaging plays
important roles in determining whether a patient is a candidate for curative
resection and in planning management.
Role of Sonography (Conventional, Contrast-Enhanced, and Intraductal)
Transabdominal sonography is commonly used to confirm the presence of bile
duct obstruction, to identify the extent of obstruction, and to determine the
cause of obstruction [9].
Dilatation of the intrahepatic bile ducts is the most frequently seen
abnormality in patients with hilar cholangiocarcinoma. Other findings depend
on the morphologic characteristics of the tumor
[9]. Papillary tumors resemble
polypoid intraluminal masses (Fig.
1A,
1B,
1C,
1D). Nodular cholangiocarcinoma
manifests as a discrete smooth mass associated with wall thickening.
Infiltrating cholangiocarcinoma is the most common type but is difficult to
evaluate with sonography. Most infiltrating cholangiocarcinomas appear as
mural and periductal soft-tissue thickening or focal irregularities of the
bile duct (Fig. 2A,
2B,
2C). Lobar atrophy and blood
vessel crowding may be useful secondary signs
[9]. Contrast-enhanced
sonography can be useful for detection and staging of hilar cholangiocarcinoma
in the postvascular phase [10]
(Fig. 3A,
3B). Intraductal sonography may
provide useful information by depicting the mucosal layers in biliary
strictures and facilitating estimation of the extent of tumor infiltration
[11] (Fig.
4A,
4B,
4C).
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Fig. 1A —63-year-old man with hilar cholangiocarcinoma. Intercostal
sonographic scan through common hepatic duct shows well-defined soft-tissue
intraductal mass (white arrow) within dilated intrahepatic duct
(black arrow). S8 = segment VIII.
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Fig. 1B —63-year-old man with hilar cholangiocarcinoma.
Contrast-enhanced CT scan barely depicts intraductal papillary tumor
(arrow). Papillary tumor is more easily seen with sonography than
with CT.
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Fig. 2A —58-year-old man with hilar cholangiocarcinoma. Subcostal
oblique gray-scale sonographic scan through porta hepatis shows abrupt
narrowing of right intrahepatic duct (black arrows) secondary to
infiltrating tumor (white arrow).
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Fig. 3A —55-year-old man with hilar cholangiocarcinoma.
Contrast-enhanced sonographic scan shows extent of tumor at hilum (black
arrows). Right hepatic artery (white arrows) and dilated duct
(arrowhead) are enhanced.
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Role of MDCT
CT is an excellent imaging technique for evaluating the soft-tissue extent
of hilar cholangiocarcinoma and the relation between the tumor and the hepatic
vasculature [7,
12,
13]. MDCT increases the speed
of scanning, decreases motion and respiratory artifacts, increases
longitudinal coverage, produces thinner scans, and enables acquisition of
isotropic images. With MDCT, volumetric data are collected that facilitate 3D
assessment of vascular structures and the biliary tree. Multiplanar
reformations are a useful supplement to routine axial scans in the diagnosis
of suspected biliary tract disease
[12,
14] (Fig.
5A,
5B,
5C,
5D). Previous reports
[15,
16] have shown the limited
utility of conventional CT in the diagnosis of tumors of the bile duct. The
detection rates are only 40–68%, and assessment of resectability is
correct in only 54% of cases. The accuracy of early-generation helical CT for
predicting resectability ranges from 50% to 60%
[13,
17]. With MDCT, biliary tumors
can be correctly identified in nearly 100% of patients
[6,
18]. The accuracy of MDCT in
prediction of resectability has improved to 74.5–91.7%
[18,
19].
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Fig. 5A —67-year-old man with hilar cholangiocarcinoma,
Bismuth-Corlette type 3a. Oblique axial reformatted (A), oblique
coronal reformatted (B and C), and curved planar (D) MDCT
scans along bile duct show tumor involves primary confluence (white
arrow, A–C) and right secondary confluence (arrow,
D). Right hepatic artery (black arrows, C) is invaded
by tumor.
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Fig. 5B —67-year-old man with hilar cholangiocarcinoma,
Bismuth-Corlette type 3a. Oblique axial reformatted (A), oblique
coronal reformatted (B and C), and curved planar (D) MDCT
scans along bile duct show tumor involves primary confluence (white
arrow, A–C) and right secondary confluence (arrow,
D). Right hepatic artery (black arrows, C) is invaded
by tumor.
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Fig. 5C —67-year-old man with hilar cholangiocarcinoma,
Bismuth-Corlette type 3a. Oblique axial reformatted (A), oblique
coronal reformatted (B and C), and curved planar (D) MDCT
scans along bile duct show tumor involves primary confluence (white
arrow, A–C) and right secondary confluence (arrow,
D). Right hepatic artery (black arrows, C) is invaded
by tumor.
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Fig. 5D —67-year-old man with hilar cholangiocarcinoma,
Bismuth-Corlette type 3a. Oblique axial reformatted (A), oblique
coronal reformatted (B and C), and curved planar (D) MDCT
scans along bile duct show tumor involves primary confluence (white
arrow, A–C) and right secondary confluence (arrow,
D). Right hepatic artery (black arrows, C) is invaded
by tumor.
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Multiphasic CT is helpful for assessment of the relation between a tumor
and the hepatic hilar structures (Fig.
6A,
6B,
6C,
6D). Arterial phase images are
useful for evaluating anatomic variations in the hepatic arteries and arterial
invasion by the tumor. Portal venous phase images emphasize the relation
between the tumor and the portal vein and adjacent hepatic parenchyma. Portal
venous involvement in cholangiocarcinoma is encasement and narrowing of the
vessel more than luminal invasion, which is usually the pattern of venous
involvement by hepatocellular carcinoma.
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Fig. 6A —67-year-old man with Klatskin's tumor, type 3a. Early
arterial (A), late arterial (B), and portal venous (C and
D) phase CT scans. Late arterial phase is used to maximize enhancement
of tumor in hilar region (arrow, B). Portal venous phase is
suitable for evaluating portal vein, adjacent liver invasion, and lymph node
metastasis (arrows, D).
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Fig. 6B —67-year-old man with Klatskin's tumor, type 3a. Early
arterial (A), late arterial (B), and portal venous (C and
D) phase CT scans. Late arterial phase is used to maximize enhancement
of tumor in hilar region (arrow, B). Portal venous phase is
suitable for evaluating portal vein, adjacent liver invasion, and lymph node
metastasis (arrows, D).
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Fig. 6C —67-year-old man with Klatskin's tumor, type 3a. Early
arterial (A), late arterial (B), and portal venous (C and
D) phase CT scans. Late arterial phase is used to maximize enhancement
of tumor in hilar region (arrow, B). Portal venous phase is
suitable for evaluating portal vein, adjacent liver invasion, and lymph node
metastasis (arrows, D).
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Fig. 6D —67-year-old man with Klatskin's tumor, type 3a. Early
arterial (A), late arterial (B), and portal venous (C and
D) phase CT scans. Late arterial phase is used to maximize enhancement
of tumor in hilar region (arrow, B). Portal venous phase is
suitable for evaluating portal vein, adjacent liver invasion, and lymph node
metastasis (arrows, D).
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The diagnostic criteria for unresectability are as follows: bilateral tumor
extension to the secondary biliary confluence with bilateral invasion of the
hepatic artery or portal vein, invasion of the long segment of the main portal
vein or the main hepatic artery, atrophy of one hepatic lobe with
contralateral vascular invasion or contralateral tumor extension to the
secondary biliary confluence, metastasis to paraaortic lymph nodes, and
distant metastasis (Fig. 7A,
7B,
7C,
7D,
7E,
7F,
7G,
7H,
7I). Depending on the anatomic
configuration of the hilar ducts, some Bismuth type 4 tumors may not be an
absolute contraindication to curative resection
[18,
20,
21]. In one study
[18], MDCT had an accuracy of
93% for arterial invasion and 86% for depiction of portal venous invasion.
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Fig. 7A —Modified T categorization in American Joint Committee on
Cancer system proposed by Memorial Sloan–Kettering group
[21]. Drawings show T1 tumors
are confined to right, left, or confluence of bile ducts without portal venous
involvement in liver atrophy.
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Fig. 7B —Modified T categorization in American Joint Committee on
Cancer system proposed by Memorial Sloan–Kettering group
[21]. Drawings show T1 tumors
are confined to right, left, or confluence of bile ducts without portal venous
involvement in liver atrophy.
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Fig. 7C —Modified T categorization in American Joint Committee on
Cancer system proposed by Memorial Sloan–Kettering group
[21]. Drawings show T2 tumors
have same attributes as T1 tumors but are accompanied by ipsilateral liver
atrophy.
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Fig. 7D —Modified T categorization in American Joint Committee on
Cancer system proposed by Memorial Sloan–Kettering group
[21]. Drawings show T2 tumors
have same attributes as T1 tumors but are accompanied by ipsilateral liver
atrophy.
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Fig. 7E —Modified T categorization in American Joint Committee on
Cancer system proposed by Memorial Sloan–Kettering group
[21]. Drawings show T3 tumors
have same classifiers as T1 tumors but have ipsilateral portal venous atrophy
without main portal vein involvement. Patients with T3 tumors are considered
poor candidates for surgery. However, some Bismuth type 4 tumors with
favorable anatomic features or short-segment invasion of main portal vein may
not be absolute contraindication to curative resection.
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Fig. 7F —Modified T categorization in American Joint Committee on
Cancer system proposed by Memorial Sloan–Kettering group
[21]. Drawings show T3 tumors
have same classifiers as T1 tumors but have ipsilateral portal venous atrophy
without main portal vein involvement. Patients with T3 tumors are considered
poor candidates for surgery. However, some Bismuth type 4 tumors with
favorable anatomic features or short-segment invasion of main portal vein may
not be absolute contraindication to curative resection.
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Fig. 7G —Modified T categorization in American Joint Committee on
Cancer system proposed by Memorial Sloan–Kettering group
[21]. Drawings show T3 tumors
have same classifiers as T1 tumors but have ipsilateral portal venous atrophy
without main portal vein involvement. Patients with T3 tumors are considered
poor candidates for surgery. However, some Bismuth type 4 tumors with
favorable anatomic features or short-segment invasion of main portal vein may
not be absolute contraindication to curative resection.
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Fig. 7H —Modified T categorization in American Joint Committee on
Cancer system proposed by Memorial Sloan–Kettering group
[21]. Drawings show T3 tumors
have same classifiers as T1 tumors but have ipsilateral portal venous atrophy
without main portal vein involvement. Patients with T3 tumors are considered
poor candidates for surgery. However, some Bismuth type 4 tumors with
favorable anatomic features or short-segment invasion of main portal vein may
not be absolute contraindication to curative resection.
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Fig. 7I —Modified T categorization in American Joint Committee on
Cancer system proposed by Memorial Sloan–Kettering group
[21]. Drawings show T3 tumors
have same classifiers as T1 tumors but have ipsilateral portal venous atrophy
without main portal vein involvement. Patients with T3 tumors are considered
poor candidates for surgery. However, some Bismuth type 4 tumors with
favorable anatomic features or short-segment invasion of main portal vein may
not be absolute contraindication to curative resection.
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Postprocessing techniques such as maximum intensity projection, multiplanar
reformation, and volume rendering allow depiction of vascular structures and
the biliary tree with or without administration of biliary contrast media
(Fig. 8A,
8B). Adding routine coronal
and sagittal reformation to standard axial images may not improve overall
diagnostic accuracy in the detection of bile duct cancer with respect to tumor
extent, vascular involvement, or resectability
[22]. However, more vigorous
use of postprocessing techniques such as oblique and curved reformation with
volume rendering may increase diagnostic confidence and has the potential to
improve diagnostic accuracy in the assessment of tumor extent along the bile
duct and of vessel invasion. MDCT cholangiography can effectively delineate
the site and cause of biliary obstruction without administration of a
cholangiographic contrast agent
[12].
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Fig. 8A —62-year-old woman with hilar cholangiocarcinoma. Oblique
coronal MDCT scan shows relation between hilar tumor (thick black
arrow) and left hepatic artery (white arrow). Hepatic metastasis
is present in segment IV (thin black arrow).
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A limitation of MDCT in the assessment of biliary tumors is that bile duct
involvement, nodal metastasis, and peritoneal metastasis can be
underestimated. The accuracy of detection of horizontal spread along the bile
duct axis has been reported to be 81% with MDCT, whereas that of vertical
spread to neighboring tissues was 100%
[23]. The sensitivity of MDCT
for nodal metastasis has ranged widely between 35% and 63%
[18,
23,
24]. Because of streak
artifacts and secondary inflammatory changes that can occur when a stent is
placed, evaluation with CT may be limited in patients with metallic stents
(Fig. 9A,
9B).
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Fig. 9A —64-year-old woman with Klatskin's tumor. Oblique coronal MDCT
scans show endoscopic retrograde biliary drainage tube (arrow) in
bile duct makes it difficult to evaluate biliary extension of tumor.
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Fig. 9B —64-year-old woman with Klatskin's tumor. Oblique coronal MDCT
scans show endoscopic retrograde biliary drainage tube (arrow) in
bile duct makes it difficult to evaluate biliary extension of tumor.
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Role of MRI, Including MR Cholangiopancreatography
MRI is an excellent imaging technique for staging cholangiocarcinoma (Fig.
10A,
10B,
10C). Many centers that deal
with large numbers of cases of cholangiocarcinoma use MRI as the imaging
technique of choice for staging for the following reasons. First, the
excellent softtissue contrast allows easier identification of the tumor and
its extent. This feature is particularly useful in the evaluation of
infiltrating tumors of the duct wall. Second, it is possible to assess the
extent of peripheral ductal involvement, which is essential for surgical
planning, owing to better visualization of these ducts with MR
cholangiopancreatography (MRCP) than with ERCP. Ducts proximal to an
obstructing cholangiocarcinoma may not adequately fill during ERCP
[25–27].
MRCP is a highly accurate method of imaging the biliary tree. The reported
accuracy in determining the extent of bile duct tumors ranges from 71% to 96%
[27–29].
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Fig. 10B —55-year-old man with hilar cholangiocarcinoma,
Bismuth-Corlette type 4. T2-weighted images show tumor encasement of right
hepatic artery (arrow, B) and hepatic parenchymal invasion
(arrowhead, C).
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Fig. 10C —55-year-old man with hilar cholangiocarcinoma,
Bismuth-Corlette type 4. T2-weighted images show tumor encasement of right
hepatic artery (arrow, B) and hepatic parenchymal invasion
(arrowhead, C).
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MRCP has several advantages over direct cholangiography, such as
noninvasiveness, no need for contrast material, and depiction of the entire
biliary tree. Furthermore, acquisition of 3D data sets is feasible with a
respiratory motion correction method. The 3D RARE technique with parallel
imaging can produce larger volume coverage, thinner sections without
interslice gaps, and a higher signal-to-noise ratio than can 2D sequences and
can allow multiplanar reformations from isotropic voxels in any arbitrary
plane to clarify anatomic relations
[30–32]
(Fig. 11A,
11B). Therefore, 3D
reconstructions may provide added information useful for preoperative surgical
planning. Use of 3D contrast-enhanced dynamic T1-weighted gradient-echo
sequences (Fig. 12A,
12B,
12C,
12D,
12E,
12F) improves depiction of the
anatomic features of the hepatic artery and portal vein compared with
conventional 2D acquisition techniques.
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Fig. 11A —54-year-old man with Klatskin's tumor, type 4.
Two-dimensional thick-slab RARE (A) and maximum-intensity-projection
(B) MR cholangiopancreatographic images obtained with 3D
navigator-triggered turbo spin-echo technique show malignant hilar
obstruction.
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Fig. 11B —54-year-old man with Klatskin's tumor, type 4.
Two-dimensional thick-slab RARE (A) and maximum-intensity-projection
(B) MR cholangiopancreatographic images obtained with 3D
navigator-triggered turbo spin-echo technique show malignant hilar
obstruction.
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Fig. 12A —67-year-old man with Klatskin's tumor. Three-dimensional
dynamic T1-weighted gradient-echo MR image in arterial phase shows relation
between right hepatic artery (white arrows) and tumor (black
arrow).
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Fig. 12B —67-year-old man with Klatskin's tumor. Three-dimensional
dynamic T1-weighted gradient-echo MR images in portal venous phase show
infiltrating tumor (arrow, C and D) and lymph node
metastasis at porta hepatis (arrows, E).
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Fig. 12C —67-year-old man with Klatskin's tumor. Three-dimensional
dynamic T1-weighted gradient-echo MR images in portal venous phase show
infiltrating tumor (arrow, C and D) and lymph node
metastasis at porta hepatis (arrows, E).
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Fig. 12D —67-year-old man with Klatskin's tumor. Three-dimensional
dynamic T1-weighted gradient-echo MR images in portal venous phase show
infiltrating tumor (arrow, C and D) and lymph node
metastasis at porta hepatis (arrows, E).
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Fig. 12E —67-year-old man with Klatskin's tumor. Three-dimensional
dynamic T1-weighted gradient-echo MR images in portal venous phase show
infiltrating tumor (arrow, C and D) and lymph node
metastasis at porta hepatis (arrows, E).
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The combined use of contrast-enhanced 3D dynamic imaging and MRCP improves
the diagnostic accuracy of preoperative staging of hilar cholangiocarcinoma
[30,
33]. The diagnostic
performance of MRI with MRCP is reported to be similar to that of MDCT
combined with direct cholangiography for assessment of biliary involvement,
vascular involvement, lymph node metastasis, and tumor resectability
[30]. Because of its excellent
tissue contrast, MRI has the potential for depicting hepatic parenchymal
invasion and metastatic lesions, improving the conspicuity of the tumors, and
facilitating evaluation of the extent of tumors and infiltration into adjacent
tissues [26].
Compared with those of MDCT, the limitations of MRI in the assessment of
biliary tumors include lower spatial resolution, longer acquisition time, and
sensitivity to motion artifacts. The usefulness of MRI may be limited in
uncooperative patients and patients with biliary stents.
Role of Direct Cholangiography (ERCP, Percutaneous transhepatic Cholangiography)
Direct cholangiography, including ERCP and percutaneous transhepatic
cholangiography (PTC), has been considered the standard of reference for
evaluating the ductal extent of the tumor by direct injection of contrast
medium into the bile ducts. Direct cholangiography provides excellent
intraluminal depiction of the causes of biliary obstruction and the anatomic
features of the bile ducts. Tissue sampling is possible by washing, brushing,
or intraductal biopsy. Therapeutic drainage also can be undertaken (Fig.
13A,
13B). Both ERCP and PTC,
however, are invasive, operator-dependent, and associated with procedural
risks, including duodenal perforation, biliary leakage, cholangitis, bleeding,
and pancreatitis [34]. In
perihilar biliary obstruction, direct cholangiography frequently does not
depict the ductal anatomic features proximal to occlusive lesions, especially
in cases of high-grade obstruction (Fig.
14A,
14B). Three-dimensional MRCP
is useful in such cases.
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Fig. 13B —61-year-old man with Bismuth-Corlette type 4
cholangiocarcinoma. Percutaneous cholangiogram shows metallic biliary stents
inserted into bilateral hepatic ducts as palliative treatment.
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Fig. 14B —63-year-old man with Bismuth-Corlette type 4
cholangiocarcinoma. Maximum intensity projection of MR
cholangiopancreatographic image clearly shows bilateral dilated hepatic ducts
proximal to hilar mass (arrows).
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Conclusion
A multiple-technique approach of sonography, MDCT, MRI and MR
cholangiopancreatography, and direct cholangiography is useful for accurate
diagnosis and planning of management of hilar cholangiocarcinoma.
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Abstract
Introduction
