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HPB, 2008; 10: 106109

REVIEW ARTICLE

Staging cholangiocarcinoma by imaging studies

V. VILGRAIN
Department of Radiology, Hopital Beaujon, Paris, France

Abstract
Cholangiocarcinoma (CCA) is an adenocarcinoma that arises from the bile duct epithelium and is observed in the entire
biliary tree (intrahepatic, hilum, and extrahepatic distal). The staging of this tumor differs depending on location. The role
of imaging in the staging of hilar CCA is to assess the extent of ductal involvement by the tumor, hepatic artery, or portal
venous involvement, the functional status and volumetric assessment of the underlying liver, and the regional or distant
tumor extension. Complete assessment is done by combining magnetic resonance (MR) cholangiography and multidetector
computed tomography (CT). Multidetector CT, in particular, is accurate for resectability and the negative predictive value
(patients with disease classified as unresectable and in whom unresectability has been confirmed) is quite high: 85100%.
The role of imaging in the staging of intrahepatic CCA is to evaluate resectability based on the tumor itself, vascular
involvement, regional and distal extension, and volumetric assessment of the contralateral liver, and to determine the
prognostic factors. These factors are mainly: tumor size, the presence of satellite nodules, vascular involvement, and lymph
nodes. CT and MR imaging (MRI) are keys and their results are comparable. In distal extrahepatic CCA due to tumor
location, staging is focused mainly on the adjacent vessels (portal vein and hepatic artery), the hepatoduodenal ligament, the
proximal and distal biliary extent, and pancreatic invasion. CT and MRI are mandatory.

Introduction
Cholangiocarcinoma (CCA) is an adenocarcinoma
that arises from the bile duct epithelium and is
observed in the entire biliary tree (intrahepatic, hilum,
and extrahepatic distal). Hilar CCA, which involves
the biliary confluence or the right or left hepatic
ducts, is the most common and accounts for 4060%
of all cases. Tumor staging of CCA is crucial,
especially in hilar tumors, because most patients
present with advanced disease and are not surgical
candidates. Therefore, the role of preoperative imaging is the highest possible accuracy in predicting
resectability.
Hilar cholangiocarcinoma
There are several staging systems for patients with
hilar CCA, most of them including extent of ductal
involvement by the tumor, hepatic artery, or portal
venous involvement, functional status and volumetric
assessment of the underlying liver, and the regional or
distant tumor extension. The goal of imaging is to

answer these questions in order to increase the


proportion of RO resections.
Ultrasound
Despite several series recommending ultrasound (US)
for staging hilar CCA, US may fail to detect hepatic
artery involvement or underestimate the extent of
ductal involvement. Therefore, US by itself is insufficient for staging work-up.
Helical CT
Technical advances such as multidetector technology,
multiphasic scanning, and millimetric collimation
have considerably improved the results of CT in the
past decade. Since 1990, more than 10 original
articles have been published on the role of helical
CT in staging hilar CCA. Helical CT has an accuracy
of 8287% in determining portal vein involvement
[14]. Moreover, the presence of lobar atrophy is
associated with lobar portal involvement is most cases.
Helical CT was considered less accurate for hepatic

Correspondence: Valerie Vilgrain, Department of Radiology, Hopital Beaujon, 100 bd du General Leclerc 92110 Clichy, France. Tel:  33 1 40 87 53 58. Fax:
 33 1 40 87 05 48. E-mail: valerie.vilgrain@bjn.aphp.fr

(Received 7 February 2008; accepted 14 February 2008)


ISSN 1365-182X print/ISSN 1477-2574 online # 2008 Taylor & Francis
DOI: 10.1080/13651820801992617

Staging cholangiocarcinoma by imaging studies

107

Table I. Summary of the results of CT and MRI in assessing vascular involvement in patients with hilar cholangiocarcinoma.

Frola [3]
Han [4]
Feydy [2]
Lee [1]
Manfredi [12]
Lee [29]

CT 1994
CT 1997
CT 1999
CT 2006
MR 2001
MR 2003

Artery Se

Artery Sp

Artery Acc

21
27
11
55
12
36

13%
25%
86%

57%
97%

62%
45%
93%

Vein Sp

71%
77%

100%
93%

58%

93%

89%

78%

91%

Vein Acc

70%

artery involvement, but recent studies have shown an


accuracy of 93% [1]. Table I indicates the respective
sensitivities, specificities, and accuracies of CT series
using helical technology. Conversely, CT has limited
sensitivity of approximately 50% for N2 metastases
[1]. CT is reliable in assessing the extent of ductal
involvement by the tumor at the primary and secondary confluence, but usually underestimates more
proximal extension. Indeed, CT cholangiography,
which includes the administration of biliary contrast
material, improves this staging.
Overall, CT has an accuracy of resectability of
between 60% and 87.5%, with the best results
published in the past 5 years (Table II). Even more
important, the negative predictive value (patients with
disease classified as unresectable and in whom unresectability has been confirmed) is quite high: 85
100% [1,57]. CT is less accurate than vascular
invasion in detecting N2 metastases, small liver
metastases, and peritoneal carcinomatosis.

Magnetic resonance imaging  magnetic resonance


cholangiography
Although the role of MRI in assessing vascular
invasion has been emphasized (Table I), the main
goal of MRI is in correctly predicting the extent of
ductal involvement.
Since the 1990s, approximately 10 original papers
have been published on MRCP in hilar CCAs, but
these studies are difficult to compare because of
varying numbers of patients and methods of reference
(ERCP, PTC, or surgical exploration).
Briefly:
. MRCP is highly feasible and allows interpretation in more than 90% of cases.

Table II. Summary of the results of helical CT in assessing resectability in patients with hilar cholangiocarcinoma.

Tillich [6] 1998


Cha [7] 2000
Lee [1] 2006
Aloia [5] 2007

Vein Se

Se

Sp

PPV

NPV

Acc

20
21
55
32

100%
100%
94%
94%

56%
60%
48%
79%

20%
50%
71%
85%

100%
100%
85%
92%

60%
71%
75%
88%

87%
82%
84%
67%
89%

. The accuracy of MRCP ranges from 81% to 96%


with the exception of one study with 67% [814].
. MRCP seems more accurate for types 1 and 2
BismuthCorlette classification than the others.
. Underestimation of the extent of ductal involvement is much more common than overestimation.
. MRCP is better than ERCP, but for some teams
PTC remains the best technique [15].
. MRCP is accurate for planning treatment in 72%
to 83% [9,10].

PET
FDG-PET was initially evaluated for the diagnosis of
CCA and even detection of this tumor in primary
sclerosing cholangitis. More recently, studies have
focused on staging. Today, FDG-PET has been
disappointing in the detection of regional lymph
node metastases, i.e. with sensitivities of just 12% to
38% [1618]. The sensitivity of FDG-PET compared
to CT is lower [17,18]. Detection of peritoneal
carcinomatosis is not good with numbers of falsepositive and false-negative cases [16,19]. On the other
hand, FDG-PET appears the best technique in
detecting distant metastases, especially when using
integrated positron emission and CT (PET/CT). Two
studies have reported that findings can result in a
change of management in 17% to 30% of patients
deemed resectable after standard work-up [18,19].
Although these results have to be confirmed by larger
series, PET may hold promise in the detection of
hidden metastases and can play an additional role in
the evaluation of resectability [20].
Intrahepatic cholangiocarcinoma
Contrary to hilar CCA, the literature on staging in
intrahepatic CCA by imaging is poor. The most
important prognostic factors in intrahepatic CCA
are: tumor size of 2 or 3 cm or more, lymph node
metastasis, multiple tumors or intrahepatic metastasis, and vascular invasion [2123]. Serosal invasion is
not considered a prognostic factor in all studies.
Multivariate analyses have shown that lymph node
metastasis, multiple tumors at presentation, symptomatic tumors, and vascular invasion are independent
factors associated with poor postoperative outcome

108

V. Vilgrain

[22,23]. Therefore the goal of imaging is to get the


best accuracy in assessing these findings. In most
cases, satellite nodules are seen at imaging (65%)
[24], usually when they are larger than 1 or 2 cm in
diameter [25]; however, in Okabayashis article,
among the 51 patients who were diagnosed preoperatively with a solitary tumor, 19 (37%) had multiple
satellite lesions in the resected specimen [23]. CT and
MRI are comparable in the detection of satellite
lesions [26].
Vascular involvement is depicted in approximately
50% of cases and more often concerns the portal
branch than the hepatic veins [25]. The presence of
segmental or lobar atrophy is strongly associated with
ipsilateral portal vein encasement. The accuracy of
CT and MRI is high, and the false-negative cases
correspond to encasement of segmental portal
branches. Although these two examinations are comparable, vascular involvement is considered more
visible on CT [26].
The overall accuracy of detecting metastastic
lymph node is 77%, and the most common error on
preoperative imaging is underestimation of nodal
involvement. Lymph nodes around the cardiac portion of the stomach and along the lesser gastric
curvature should be examined in addition to nodes
in the hepatoduodenal ligament in intrahepatic
CCA of the left lobe [27]. Although rarely reported
in the staging of intrahepatic CCA, PET imaging
may be helpful in demonstrating extrahepatic metastases.

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References

Staging of extrahepatic CCA is challenging because


this tumor tends to spread outside the wall of the bile
duct and attention has to be paid to the adjacent
vessels (portal vein and hepatic artery), the hepatoduodenal ligament, the proximal and distal biliary
extent, and pancreatic invasion. CT and MRI are
mandatory. 3D angiography and multiphase fusion
images using MDCT may be useful tools [28].
Endoscopic sonography and, more recently, intraductal ultrasonography using a higher frequency have
been reported in small series.
In conclusion, imaging is important in staging
CCAs. Indications of each modality are well established for hilar CCA but less so for the other sites.

Extrahepatic distal cholangiocarcinoma

Staging cholangiocarcinoma by imaging studies


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