World J Gastrointest Oncol 2013 July 15; 5(7): 115-126

ISSN 1948-5204 (online)

Online Submissions: http://www.wjgnet.com/esps/

wjgo@wjgnet.com
doi:10.4251/wjgo.v5.i7.115

2013 Baishideng. All rights reserved.

TOPIC HIGHLIGHT
Jos M Ramia, MD, PhD, Series Editor

Radiological diagnosis and staging of hilar

cholangiocarcinoma
Carlos Valls, Sandra Ruiz, Laura Martinez, David Leiva
Carlos Valls, Sandra Ruiz, Laura Martinez, David Leiva, Department of Radiology, Bellvitge University Hospital, Barcelona
08907, Spain
Author contributions: All the authors contributed to the conception, design and interpretation of data and participated in drafting
the manuscript, revised it critically and approved the final version; the detailed writing process and analysis of the data was
performed by Valls C.
Correspondence to: Dr. Carlos Valls, Department of Radiology,
Bellvitge University Hospital, Feixa Llarga s/n L'Hospitalet de Llobregat, Barcelona 08907, Spain. carlosvalls@bellvitgehospital.cat
Telephone: +34-93-3357011 Fax: +34-93-3359011
Received: January 8, 2013
Revised: June 5, 2013
Accepted: June 18, 2013
Published online: July 15, 2013

2013 Baishideng. All rights reserved.

Key words: Cholangiocarcinoma; Radiological staging;

Magnetic resonance imaging; Multidetector computed
tomography; Hepatic resection
Core tip: Hilar cholangiocarcinoma is a rare malignant
tumor arising from the epithelium of the bile ducts.
Surgery is still the only chance of potentially curative
treatment in patients with perihilar cholangiocarcinoma.
Multidetector computed tomography, magnetic resonance imaging and magnetic resonance cholangiography are useful tools, both to diagnose and stage hilar
cholangiocarcinoma.
Valls C, Ruiz S, Martinez L, Leiva D. Radiological diagnosis
and staging of hilar cholangiocarcinoma. World J Gastrointest
Oncol 2013; 5(7): 115-126 Available from: URL: http://www.
wjgnet.com/1948-5204/full/v5/i7/115.htm DOI: http://dx.doi.
org/10.4251/wjgo.v5.i7.115

Abstract
Hilar cholangiocarcinoma is a rare malignant tumor
arising from the epithelium of the bile ducts. Surgery
is still the only chance of potentially curative treatment
in patients with perihilar cholangiocarcinoma. However,
radical resection requires aggressive surgical strategies
that should be tailored optimally according to the location, size and vascular invasion of the tumors. Accurate
diagnosis and staging of these tumors is therefore critical for optimal treatment planning and for determining a
prognosis. Multidetector computed tomography (MDCT),
magnetic resonance imaging (MRI) and MR cholangiography are useful tools, both to diagnose and stage
hilar cholangiocarcinoma. Modern imaging techniques
allow accurate detection of the level of obstruction and
the longitudinal and radial spread of the tumor. In addition, high-resolution MDCT and MR provide specific
radiographic features to determine vascular involvement
of anatomic structures, such as the hepatic artery or
the portal vein, which are critical to decide the surgical
strategy. Finally, radiological staging allows detection of
patients with distant metastasis in the liver or peritoneum who will not benefit from a surgical approach.

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INTRODUCTION
Carcinomas of the extrahepatic biliary tree, commonly
known as hilar cholangiocarcinoma (HCCA), Klatskin tumors or perihilar cholangiocarcinomas, are rare malignancies that account for up to 3% of all gastrointestinal cancers. With an incidence rate of 0.5-2.0 cases per 100000,
it is estimated that there are between 2500 and 4000 new
cases per year in the United States[1].
Although this tumor may potentially affect any location of the biliary tree, tumors involving the biliary
confluence, left-hand drive (LHD) and right-hand drive
(RHD) (true Klatskin tumors) are most common and
account for 40%-60% of all cases. Around 2/3 of cholangiocarcinomas are hilar or extrahepatic and originate
from the bile duct epithelium at the level of confluence

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of the right and left ducts, whereas 30% are distal or

intrapancreatic and 5%-10% are intrahepatic[2]. Due to
recent improvements in radiological techniques, there is
a wide range of imaging tools available for diagnosis and
staging HCCA, such as multidetector computed tomography (MDCT), magnetic resonance (MR), endoscopic
ultrasonography, endoscopic retrograde cholangio pancreatography (ERCP) and angiography. However, to date,
there is no consensus as to the best staging algorithm.
The aim of this paper is to review the results in the preoperative staging of HCCA with modern non-invasive
imaging techniques, including MDCT, magnetic resonance imaging (MRI) and MR cholangiopancreatography
(MRCP).

such as primary sclerosing cholangitis (PSC), although

the vast majority of cancers are seen in patients with no
readily identifiable predisposing condition. PSC is an autoimmune condition that causes bile duct inflammation
resulting in scarring and fibrosis. This chronic inflammation is thought to lead to dysplastic and ultimately
neoplastic changes in the bile ducts. The risk of cholangiocarcinoma in patients with PSC is thought to be
over a 1000-fold higher than in the general population
and is thought to be 0.5%-1.0% per year or 10%-40%
lifetime risk[7]. While both intrahepatic and extrahepatic
cholangiocarcinoma are well-known complications of
PSC in Western countries, hepatolithiasis, infections due
to liver flukes and bile stasis are risk factors strongly
associated with cholangiocarcinoma in Eastern Asia.
However, approximately 90% of patients diagnosed with
cholangiocarcinoma do not have a recognized risk factor
in Western countries[8]. Other risk factors include an abnormal choledochopancreatic junction, choledocal cyst,
ulcerative colitis, cirrhosis, alcoholic liver disease, type
diabetes, thyrotoxicosis, pancreatitis and possibly duodenal ulcer disease[9].

PATHOLOGICAL AND CLINICAL

FEATURES
Cholangiocarcinoma is a malignant tumor arising from
bile duct epithelium of any portion of the biliary tree. It
is the second most common primary liver cancer in the
world, except for certain areas where it is more common
than hepatocellular carcinoma (HCC). Traditionally, it has
been classified as an intrahepatic and extrahepatic tumor
according to its location with respect to the liver; this
last category has been subdivided into upper, middle and
distal by its location. However, recent literature classifies
extrahepatic cholangiocarcinoma into perihilar and distal
cancer, due to the relatively low incidence of middle bile
duct cancer[2], and the correlation of these categories with
anatomic distribution and preferable treatment. Perihilar
cholangiocarcinoma, also called Klatskin tumors[3], can be
defined as tumors originating on the right or left duct, near
their junction or in close vicinity to the bile duct confluence, and represent two-thirds of cholangiocarcinomas[4].

Clinical features
Obstructive jaundice is the main clinical feature and can
appear relatively early, even with small neoplasms. It may
progress rapidly or fluctuate. Other symptoms may include weight loss, pruritus, right-upper quadrant pain or
fever and chills if cholangitis develops.

DIAGNOSIS OF HCCA
Imaging techniques
The majority of patients with HCCA present with severe
painless jaundice as the initial clinical presentation. However, not every patient with jaundice and biliary obstruction at the hepatic hilus will eventually be confirmed as
HCCA. In fact, almost 25% of cases turn out to have
other benign conditions (such as lymphoplasmacytic
cholangitis or Mirizzi syndrome) or other malignant disease (such as gallbladder cancer or nodal metastasis) that
has obstructed the hepatic confluence[10].
Initial radiological assessment is performed with
sonography in most patients with perihilar biliary tract
malignancies. Ultrasound rarely allows direct demonstration of perihilar biliary cancer, although indirect signs
such as isolated intrahepatic dilatation can be useful in
suggesting the diagnosis. However, in most cases, additional diagnostic procedures are necessary to confirm the
diagnosis. The main goals of imaging in that setting will
be to differentiate HCCA from other conditions leading
to obstructive jaundice with intrahepatic dilatation and
to perform an accurate preoperative evaluation of tumor
resectability, focusing on vascular and biliary invasion as
well as invasion and distant metastasis to the liver and
lymph nodes. In the past, direct cholangiography combined with angiography was used to assess tumor extension. More recently, the advent of MDCT and MRCP has

Pathology
Most cholangiocarcinomas are adenocarcinomas with
variable differentiation grades and fibroplasia. According
to the last World Health Organization (WHO) histological classification, different types of adenocarcinoma are
considered, and precursor lesions such as biliary intraepithelial neoplasia and intraductal papillary neoplasms
are also included[5]. Macroscopically, carcinomas of the
extrahepatic bile ducts have been divided into polypoid,
nodular, scirrhous constricting and diffusely infiltrating
types. These categories can provide a guide to the operative procedure, extent of resection and prognosis. However, except for the polypoid type, this division is rarely
possible due to overlapping on gross features. However,
the nodular and scirrhous types which tend to coexist are
prone to infiltrate surrounding tissues, while the diffusely
infiltrating type tends to spread linearly along the ducts.
Epidemiology and risk factors
Cholangiocarcinoma occurs with a highly varying frequency in different areas of the world [6]. There are
several recognized risk factors for cholangiocarcinoma,

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dramatically changed the imaging evaluation of patients

with hilar cholangiocarcinoma.
The role of cholangiography in the evaluation of
hilar cholangiocarcinoma is two-fold: to assess tumoral
extension to identify potentially resectable patients and
to help in planning palliative biliary drainage in nonresectable patients. In this clinical setting MRCP has a
number of potential advantages over ERCP and transhepatic cholangiography (THC). MRCP allows rapid
non-invasive evaluation of the biliary tract without instrumentation and therefore without the risk of inducing
sepsis in patients with ductal obstruction. Additionally,
MRCP depicts tumoral extension along the intrahepatic
branches of the biliary tree more consistently than
ERCP and THC, especially in high grade stenosis[11]. In
Fulchers series[12], MRCP allowed a more detailed visualization of the bile ducts than direct cholangiography
in 3 of 4 patients who underwent both techniques. In
another study, Holzknecht et al[13] performed a prospective comparison of MRCP and ERCP in 61 patients
who underwent ERCP for a variety of clinical indications. ERCP demonstrated 36 stenosis in 33 patients
(15 malignant and 21 benign). MRCP diagnosis was
correct in 89% of the cases (32/36) and there were 4
false negative findings. However, MRCP was correct in
all 15 patients with high-grade malignant stenosis. On a
patient-by-patient basis, statistical analysis to compare
the grade of stenosis indicated that differences between
MRCP and ERCP were not significant. In a recent study
by Yeh et al[14], the efficacy of MRCP and ERCP in 40
patients with malignant perihilar obstruction, including
26 patients with Klatskin tumor, were compared. ERCP
was unsuccessful in 2 patients. In this series, MRCP was
superior to ERCP in delineating the anatomic extent of
the tumoral lesions: 34/40 vs 24/38. Therefore, direct
cholangiography, either endoscopic or percutaneous,
has been definitively abandoned as a diagnostic tool and
substituted by MRCP.
MDCT allows for faster scanning with thinner collimation and results in an improved diagnosis and staging
hilar cholangiocarcinoma. CT is usually performed to
assess the level of biliary obstruction (longitudinal extension) as well as involvement of liver parenchyma and
vascular hilar structures (radial extension). High resolution CT allows for accurate depiction of a thickened bile
duct wall and tumor spread into liver parenchyma or hilar
vessels and therefore plays a key role in the diagnosis and
staging of HCCA. Previous results of conventional CT
in the diagnosis and staging of hilar cholangiocarcinoma
have been limited. The advent of helical technology has
dramatically improved the results of CT in the detection
and diagnosis of Klatskin tumors, although its ability to
perform an accurate staging is still limited. In the series
by Tillich et al[15], HCT correctly detected all hilar cholangiocarcinomas using a biphasic technique. However, its
overall accuracy for predicting resectability was only 60%.
In Feydys series[16], HCT correctly detected and localized
the mass in 91% of the cases.

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Figure 1 Mass forming cholangiocarcinoma. Axial computed tomography

scan in the portal phase (A) and in delayed phase (B) shows a heterogeneous
hypovascular mass (arrow) with rim-like peripheral enhancement. The lesion is
associated with ductal infiltration and biliary dilation.

Diagnostic features
Diagnostic features of HCCA include intrahepatic segmental biliary dilatation, periductal thickening, endoluminal lesions and direct tumor spread to the liver or adjacent vessels. Biliary dilatation is usually intrahepatic and
often segmental and located proximally to an ill-defined
biliary mass near the hepatic hilus. The transition between dilated and non dilated bile ducts is usually abrupt
and this is a key feature for diagnosis. Therefore, these
patients should not be drained before an adequate imaging study is performed.
On the basis of the Japanese Liver Cancer Group[17]
classification, cholangiocarcinomas are classified into
three types: mass-forming, intraductal growing and periductal infiltrating. The latter is the most prevalent in the
hilar portion of the biliary tree and forms the majority of
perihilar cholangiocarcinomas.
Mass-forming cholangiocarcinoma: In some cases,
HCCA presents as a mass-forming lesion (Figure 1).
This pattern of presentation includes periductal thickening and a solid tumor lesion involving the adjacent liver
parenchyma[18]. Mass-forming intrahepatic cholangiocarcinoma is usually a bulky lesion with infiltrating features
around the adjacent peripheral branches of the portal
vein. On CT and MRI, mass-forming HCCA are usually
heterogeneous hypovascular masses with rim-like peripheral enhancement in the arterial and portal phase and
delayed enhancement in the equilibrium phase. These

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A

L
R

Figure 2 Intraductal growing cholangiocarcinoma. A: Axial computed tomography in

the portal phase in a 52-year-old male shows
a heterogeneously enhancing endoluminal
lesion with dysmorphic calcifications (arrow).
Note biliary dilatation upstream; B: Coronal
thin-slab (echo spacing 4.2 ms, effective echo
time 183 ms, image matrix 272 x 512, FOV
385 mm) T2-W sequence shows marked
dilatation of the common hepatic duct and a
hypointense endoluminal mass (arrow); C:
Axial thin-slab (echo spacing 4.2 ms, effective echo time 183 ms, image matrix 272 x
512, FOV 385 mm) T2-W sequence shows
a hypointense filling defect consistent with
polypoid cholangiocarcinoma in the common
hepatic duct (arrow).

enhancement features reflect the nature of the tumor,

which is mainly desmoplastic. The bile ducts peripheral
to the tumor are usually dilated because of obstruction
by the tumor.

mass on imaging studies. However, with the advent of

MDCT, thin-collimation tumoral periductal involvement
is almost always detectable. High-resolution CT shows
tumoral involvement as an irregular periductal thickening
completely obstructing or narrowing a short segment of
the biliary tree around the biliary bifurcation or common
hepatic duct (Figure 3).
Periductal thickening is usually iso-hypo enhancing
in arterial and portal phases and shows marked enhancement on delayed phase imaging (Figure 4). Occasionally
periductal thickening may show brisk hyperenhancement in
the arterial phase, mimicking endobiliary HCC (Figure 5).
On MRCP, non union of the right and left hepatic ducts
is a typical finding of infiltrating hilar cholangiocarcinoma.

Intraductal growing cholangiocarcinoma: In intraductal growing cholangiocarcinoma, bile ducts can be

dilated because of tumoral obstruction, increased mucin
secretion or sloughed tumor debris. This pattern of cholangiocarcinoma is frequently found in papillary cholangiocarcinomas (Figure 2). On imaging, the involved bile
ducts are asymmetrically dilated. Typically, an endoluminal mass is found in the segment with more intense
dilatation. Intraductal cholangiocarcinoma is confined in
the lumen of the dilated bile duct without direct tumoral
extension to the surrounding liver parenchyma. This pattern of spread is radically different from mass-forming
or periductal infiltrating cholangiocarcinoma that typically
shows marked infiltration. This is related to the different
histological patterns of the tumors. Intraductal growing
cholangiocarcinoma appears as a nodular, well defined
mass on CT or MR and typically shows intense enhancement after contrast injection. The mass is confined within
the bile ducts and therefore there is preservation of the
bile duct wall[18].

Differential diagnosis
There is a wide variety of benign and neoplastic lesions
at the liver hilum that may cause biliary stricture. In particular, inflammatory lesions may present with the same
radiological features as those from malignant tumoral
causes.
The most frequent benign lesions that may mimic
cholangiocarcinoma include lymphoplasmacytic cholangiopathy (IgG4 sclerosing cholangitis), endobiliary metastases, endobiliary HCC and Mirizzi Syndrome.
Several studies have noted that approximately 14% to
25% of resected patients for cholangiocarcinoma (HCCA)
prove to have a benign lesion at histopathology[19,20]. Differentiation between malignant and benign strictures in
patients with suspicion of cholangiocarcinoma is often
impossible before laparotomy due to overlapping of radiological and clinical features. In addition, there are no
specific radiological or laboratory tests that may distin-

Periductal infiltrating cholangiocarcinoma: This pattern of cholangiocarcinoma is frequently found in perihilar cholangiocarcinoma. Periductal infiltrating cholangiocarcinoma typically shows marked dilatation on imaging
of the biliary tree proximal to the tumoral lesion. On CT,
the involved bile ducts are diffusely narrowed or obliterated. With conventional helical or incremental CT it was
extremely difficult or impossible to depict the tumor

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Figure 3 Periductal cholangiocarcinoma multidetector computed tomography. A: Multidetector computed tomography (MDCT) in the portal phase at the level of
the hepatic hilus shows an irregular periductal thickening completely obstructing the common hepatic duct consistent with periductal cholangiocarcinoma (arrow). The
lesion is hypoenhancing in the portal phase; B: Delayed phase MDCT at the same level shows marked hyper-enhancement of the tumoral lesion (arrow).

Figure 4 Periductal cholangiocarcinoma

multidetector computed tomography
and magnetic resonance cholangiopancreatography. A: Multidetector computed
tomography in the portal phase shows periductal cholangiocarcinoma (arrow) producing complete biliary obstruction and atrophy
of the right liver; B: Coronal reconstruction
shows to a better advantage the scirrhous
infiltrating cholangiocarcinoma slightly hyperenhancing (arrow) and the dilated bile
ducts upstream; C: Coronal thick-slab (echo
spacing 8.3 ms, effective echo time 1000 ms,
image matrix 512 x 512, FOV 350 mm)
MRCP T2-W sequence in the same patient
shows marked dilatation of intrahepatic bile
ducts and a signal void (arrow) at the level
of the hepatic convergence and common
hepatic duct consistent with malignant obstruction by cholangiocarcinoma; D: Matrix
(272 x 512, FOV 385 mm) T2-W sequence
shows marked dilatation of the intrahepatic
ducts and a narrow stenosis at the hepatic
bifurcation (arrow).

guish HCCA from benign proximal bile duct lesions.

Malignant stricture is characterized by bile-duct wall
thickening greater than 1.5 mm, arterial and venous hyperenhancement of the stricture, and greater extent of
proximal dilatation compared with benign lesions[21]. Different imaging studies have shown that only one feature,
vascular involvement, was significantly different in benign
and malignant lesions[22].

of serum immunoglobulin G4. IgG4-sclerosing cholangitis shows clinical response to steroid therapy. Prompt initiation of steroid treatment in these patients could greatly
improve outcomes, at least in part by avoiding unnecessary surgery. Both the intrahepatic and extrahepatic segments can be involved by lymphoplasmacytic infiltration
characterized by transmural fibrosis which may extend to
the periportal area of the liver, causing biliary stricture[24].
A stricture of the distal CBD is the most common
abnormality of IgG4 sclerosing disease, reported in
54%-79% cases[25,26]. Associated imaging findings of autoimmune pancreatitis, such as focal or diffuse pancreatic
enlargement with a peripheral ring of low attenuation and
a diffusely narrowed pancreatic duct, are useful features
in pointing the diagnosis of autoimmune cholangitis[26].
However, accurate preoperative diagnosis of lymphoplasmacytic cholangitis and differentiating this condition from hilar cholangiocarcinoma is still very difficult

Lymphoplasmacytic cholangiopathy
IgG4-sclerosing cholangitis is considered part of IgG4
systemic-related diseases and is commonly associated
with autoimmune pancreatitis[23]. The occasional absence
of pancreatic involvement in these patients has been previously reported. No strict diagnostic criteria have been
described to date and diagnosis relies on a combination
of clinical and histopathological findings. A typical diagnostic feature of IgG4-sclerosing cholangitis is elevation

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Figure 5 Hypervascular periductal cholangiocarcinoma. A: Multidetector computed tomography shows

periductal cholangiocarcinoma with brisk arterial enhancement in the arterial phase (arrow); B: Portal phase
multidetector computed tomography at the same level
shows mild tumoral enhancement (arrow).

Figure 6 Lymphoplasmacytic cholangiopathy multidetector computed tomography. A: Multidetector computed tomography (MDCT) in the
portal phase shows marked intrahepatic dilatation and marked irregular
thickening of the common hepatic duct; B: MDCT in the same patient more
caudally shows abrupt stenosis and obliteration of the bile duct lumen.
Surgical exploration confirmed lymphoplasmacytic cholangiopathy.

because of the overlapping imaging features of both

conditions (Figures 6 and 7). Both HCCA and LC have
a similar gross macroscopic appearance related to their
fibrous nature.

HCC may be related to blood clots, sludge or intrabiliary

tumoral growth. In the absence of gallbladder stones,
the most frequent cause of intrabiliary filling defects is
HCC.
Intrabiliary growth of HCC shows the same enhancement pattern as the primary tumor and is hyperenhancing
in the arterial phase with wash-out in portal and delayed
phases. Occasionally, endobiliary growth of HCC may
be found in patients without a definite hepatic mass[28].
In that setting, the differential with intraductal growing
cholangiocarcinoma may be very difficult with imaging,
although a clinical setting of chronic liver disease may
suggest the diagnosis.

Endobiliary metastases: Neoplastic intraductal filling

defects are usually considered primary intraductal biliary
neoplasms until they are proved otherwise pathologically.
Nevertheless, it is also well-known that extrabiliary malignant tumors, such as lung, breast, gallbladder, colon,
testis, prostate, pancreas, melanoma and lymphoma, can
metastasize to the bile duct and manifest as an intraductal
mass too. When an intraductal lesion is found in a patient
with extrabiliary malignancy, the presence of a contiguous parenchymal mass, an expansible nature of the intraductal lesion, and a history of colorectal cancer may
suggest the presence of intraductal metastasis rather than
double primary intraductal cholangiocarcinoma[27].
However, occasionally endobiliary metastases can be
isolated without associated liver metastases and only the
clinical setting may help in the differential diagnosis (Figure 8).

Mirizzi syndrome: Mirizzi syndrome is a form of obstructive jaundice caused by a bile duct stone impacted
in the neck of the gallbladder or in the cystic duct. The
stone and surrounding inflammation compress the
common hepatic duct and results in dilation of the bile
ducts upstream[29]. This is a rare complication of cholelithiasis. An accurate diagnosis is essential for proper
management of a patient. From a pathophysiological
point of view, Mirizzi syndrome may have two causes.
In Mirizzi type there is chronic inflammation of
the gallbladder with marked contraction of the fibrous
gallbladder wall that adheres to the common bile duct,
resulting in fibrous stenosis of the biliary lumen. In
Mirizzi type there is a direct cholecysto-biliary fistula
secondary to direct compression of large stones on the
wall of the common hepatic duct. Imaging reveals dilated intrahepatic bile ducts with a normal common bile
duct. The gallbladder is usually collapsed. The diagnosis

HCC with endobiliary growth: Obstructive jaundice

as the main clinical feature is uncommon in patients
with HCC. Only 1%-12% of HCC patients present with
obstructive jaundice as the initial complaint. HCC may
involve the biliary tract in several different ways: tumor
thrombosis, hemobilia or endoluminal tumor extension.
Jaundice in patients with HCC is usually related to diffuse tumoral intrahepatic extension with hepatic insufficiency. Filling defects in the biliary tree in a patient with

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Figure 7 Lymphoplasmacytic cholangiopathy multidetector computed tomography and magnetic resonance cholangiopancreatography. A, B: Coronal reconstructed and axial multidetector computed tomography in the portal phase show periductal thickening of the common hepatic duct and hepatic bifurcation (arrows); C:
Coronal thin-slab (echo spacing 4.2 ms, effective echo time 183 ms, image matrix 272 x 512, FOV 385 mm) T2-W sequence shows marked intrahepatic biliary dilatation and an abrupt stenosis of the coronary heart disease and biliary bifurcation (arrows); D: Coronal thick-slab (echo spacing 8.3 ms, effective echo time 1000 ms, image matrix 512 x 512, FOV 350 mm) magnetic resonance cholangiopancreatography T2-W sequence in the same patient shows marked dilatation of intrahepatic bile
ducts and a signal void in the hepatic bifurcation mimicking Klatskin tumor. Surgical exploration and histological study confirmed lymphoplasmacytic cholangiopathy.

Figure 8 Endobiliary metastases. Sixty eight-year-old patient with obstructive jaundice. The patient had been operated on for liver metastases of colorectal cancer
3 years ago (right hepatectomy). A, B: Portal phase computed tomography shows left intrahepatic biliary dilatation (arrowheads) and a solid slightly hyperenhancing
endoluminal mass in the left hepatic duct; C: Coronal reconstruction shows to a better advantage the fluid density of dilated bile ducts and the solid density of the endobiliary tumor (arrows). Percutaneous fine-needle aspiration biopsy confirmed endobiliary metastasis.

may be suspected on CT when calcified bile stones are

detected. However, in most cases stones are radiolucent
and not detectable with CT. MRCP is the most efficient
imaging technique in this setting, allowing detection of
impacted stones at the gallbladder neck with compression of the hepatic duct and upstream biliary dilatation.
The treatment of Mirizzis syndrome may be a simple
cholecystectomy with or without hepaticojejunostomy
in case of fistula.

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PREOPERATIVE STAGING AND

ASSESSEMENT OF RESECTABILITY
Cholangiocarcinoma is one of the most difficult tumors,
both to stage and treat. Surgery remains the only curative treatment for HCCA. However, surgical treatment
of this malignant tumor is impaired by the lack of an
effective adjuvant treatment. In addition, the specific anatomic location of these tumors usually involving critical

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is to resect the whole tumor with free margins but still

leave enough liver to maintain hepatic function. This is
particularly difficult in HCCA due to its infiltrating nature. Preoperative staging should focus on biliary, vascular, hepatic, lymph node and extrahepatic extension.
Unresectability criteria generally include liver metastasis, distant lymph node metastasis, bilateral arterial or portal invasion, unilateral vascular invasion and contralateral
lobar atrophy and distant metastases. Parenchymal invasion is not considered an unresectability criterion because
a right or left hepatectomy can be performed. Bismuth
stage is also not always considered an unresectability
criterion because with an extra-Glissonian approach and
hepatectomy some lesions can be safely resected.

Longitudinal extension of cholangiocarcinoma: Biliary

staging
Biliary extension is usually assessed with MRCP. MRCP
can confidently classify cholangiocarcinoma according to
the Bismuth-Corlette Classification in stages, , a,
b and (Figure 9). Stage includes tumor confined
to the common hepatic duct. Stage includes tumor involving the confluence of the right and left hepatic ducts
without proximal biliary involvement. Stage a includes
tumor involving the confluence of the right and left hepatic ducts with proximal extension to the confluence
of the anterior and posterior right segmental bile ducts.
Stage b includes tumor involving the confluence of the
right and left hepatic ducts with proximal extension to
the confluence of bile ducts for segments and -.
Bismuth stage includes tumor involving the confluence of the right and left hepatic ducts with proximal
extension to both secondary confluences of the right and
left hepatic ducts.
In the paper by Maselli et al[32], fifteen patients with hilar cholangiocarcinoma underwent radical surgery and preoperative MR imaging. MRCP and gadolinium-enhanced
dynamic T1-W images were correlated with surgical findings in the evaluation of the extent of biliary infiltration
according to the Bismuth-Corlette classification.
Radiological-pathological correlation disclosed that the
assessment of the bile duct stenosis by MRCP alone was
correct in 80% of the patients (12/15). MRCP underestimated tumor spread in two patients who were considered
preoperatively type and type A and turned out to be
type A and respectively at surgical exploration.
MRCP overestimated the neoplastic biliary extent in
another patient who was considered type a preoperatively and was proven to be type at histology. Overall
accuracy for MRCP to classify tumor according to the Bismuth Classification was 80%. In the series by Lee et al[33],
longitudinal biliary involvement was accurately predicted
with MDCT in 84% of the patients.

Figure 9 Bismuth-Corlette classification.

vascular structures makes complete resection extremely

challenging. This is a critical point because long-term
survival in patients with HCCA depends on complete
tumor resection. Due to the infiltrative growth pattern
of HCCA, thorough preoperative evaluation of the extent of tumor along the biliary tree and major vessels at
the hepatic hilum is needed in order to plan adequate
surgical treatment. Initial reports on surgical resection
of cholangiocarcinoma involved only patients treated
with biliary resection with hepaticojejunostomy with
poor survival benefits[30]. Experience over recent years
has shown a dramatic increase of radical surgical procedures with extended right or left hemi-hepatectomies,
reporting 5-year survival rates between 25% and 40%[31].
In addition, development of sophisticated preoperative
imaging techniques with multiplanar, biliary and vascular
reconstructions has improved the depiction of both direct radial hepatic invasion and longitudinal intraductal
extension of cholangiocarcinoma. The main problem until now has been the poor results of preoperative staging
methods in order to separate potentially resectable from
non-resectable patients and to avoid unnecessary surgical
procedures, because benefits in terms of survival are only
achieved if the tumor is completely resected.
The cornerstone of oncological resection in the liver

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Radial extension of cholangiocarcinoma: Vascular

staging
Vascular extension is either assessed with MDCT or gadolinium-enhanced dynamic MRI. Accurate preoperative
assessment of HCCA requires thorough evaluation of

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Valls C et al . Radiological diagnosis and staging of hilar cholangiocarcinoma

Figure 10 Liver infiltration of cholangiocarcinoma. A: Coronal reconstructed multidetector computed tomography shows a periductal mass at the hepatic
confluence consistent with cholangiocarcinoma (arrow); B: Axial computed
tomography of the same patient shows a hypoenhancing mass involving the
liver parenchyma and hilar vessels (arrow) consistent with tumoral infiltration by
cholangiocarcinoma.

Figure 11 Portal infiltration of cholangiocarcinoma. A: Axial computed tomography in the portal phase shows a periductal mass in the portal confluence
(arrowheads) producing biliary dilatation (arrows); B: The mass extends cranially and shows encasement and infiltration of the left portal vein.

be unresectable (NPV: 50%), although none of them was

related to vascular invasion (lymphadenopathy, metastasis,
intraductal extension and anatomic variants).
In Masellis series[32], MRI correctly predicted vascular
involvement in 73% of the cases. MR correctly showed
arterial involvement in 88% of the cases (8/9) and had
false positive findings in 12% (1/9). Portal invasion was
correctly assessed in 73% of the cases (11/15) and underestimated in 20% of the cases (3/15). In 7% of the
patients (1/15), portal vein invasion was overestimated
and not confirmed by histology.
In the series by Lee et al[33], the accuracy of MDCT in
the prediction of portal vein and hepatic artery invasion
was 85.5% and 92.7% respectively. Overall accuracy of
resectability was 74.5%.
In Chryssous series[35], preoperative dynamic MRI
with gadolinium was fully concordant with surgical
data in the assessment of tumoral invasion in 77% of
the veins studied (63/82) and in 58% (43/74) arteries. Concordance was better concerning the assessment
of venous invasion but several cases with discordance
were reported in that series. MRI showed no tumoral
involvement in 5 cases but surgical exploration suggested
tumoral infiltration. These veins were resected but final
histological study showed no tumor infiltration.
In addition, only 60% of the veins with suspected tumor infiltration on MR and survival exploration showed
definite microscopic wall invasion at histological study.
However, those lesions would probably not have been

the hepatic artery (right, left and common hepatic artery)

and portal veins (right, left and main portal vein) (Figures
10 and 11).
MDCT and MRCP are useful techniques to delineate
the extent of the tumor and to rule out vascular invasion and locoregional lymph node extension. Helical CT
should be performed to rule out liver and lymph node
metastasis as well as vascular encasement but proximal
tumor extent along bile ducts is often underestimated.
On the other hand, helical CT also plays a key role
in the management and staging of cholangiocarcinoma.
HCT allows assessment of tumor spread to the liver or
regional
lymph nodes, as well as arterial or portal involve[15]
ment . Previous results of conventional CT in the diagnosis and staging of hilar cholangiocarcinoma have been
limited. The advent of helical technology has dramatically
improved the results of CT in the detection and diagnosis
of Klatskin tumors, although its ability to perform an ac[15]
curate staging is still limited. In the series by Tillich et al ,
HCT correctly detected all hilar cholangiocarcinomas
using a biphasic technique. However, its overall accuracy
for predicting
resectability was only 60%. In a study by
[34]
Cha et al , 21 patients with perihilar cholangiocarcinoma
were studied with MDCT. CT correctly detected that
the tumor was unresectable in 8 cases (PPV: 100%), due
to vascular involvement in 8 cases and distant lymphnode metastases in 1 case. However, in 12 patients with
suspected resectable disease by CT, 6 cases turned out to

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Valls C et al . Radiological diagnosis and staging of hilar cholangiocarcinoma

resectable without vascular resection.

Some surgical studies[36] have reported that tumoral
involvement of portal veins may be overestimated by surgical exploration compared with histology because there
was no adventitial tumoral invasion. These studies reflect
the challenges of vascular staging of hilar cholangiocarcinoma. In most cases, there is close contact between
the tumor and the venous or arterial structure and it is
difficult to determine if it is invaded or not. In our experience, only complete tumor encasement (tumor contact
with the vessel of more than 50%) is an adequate sign
to predict tumor invasion. Despite the fact that in some
cases the wall of the vein is actually not invaded microscopically by tumor, the fact is that the tumor cannot be
resected without resecting the vessel. In cases of minor
tumoral abutment, the patient should not be considered
unresectable and surgery should be performed.
In Chryssous series[35], 80% of non-stented patients
with tumor-to-portal vein contact of more than 90% but
without stenosis on MR had invasion of the adventitia
confirmed histologically. This may be a useful criterion
for predicting invasion of the portal vein or its segmental
branches in non-stented patients. In the same series[35],
the excellent correlation between MRI and surgery was
associated with a weaker correlation between MRI and
pathology. These results reflect that both MRI and surgery have limitations in differentiating true microscopic
invasion from adherent perivascular fibrosis. This kind
of fibrosis is especially frequent in patients with previous biliary drainage because at the hepatic hilus there is
close anatomic contiguity between the vessels and the
biliary tree. Therefore, in patients with suspected perihilar
cholangiocarcinoma it is critical that biliary intervention
should be avoided before an adequate preoperative staging is performed. Invasion of adjacent liver parenchyma
is also critical in order to assess resectability of cholangiocarcinoma. In mass forming cholangiocarcinoma,
parenchymal infiltration is readily seen because tumor
has an eccentrical location related to bile ducts. However,
in periductal cholangiocarcinoma, parenchymal infiltration may be subtle and high-resolution thin collimation
scanning is needed. Imaging with MDCT or MRI shows
a hypovascular infiltrating tumoral mass growing beyond
the duct and invading the adjacent liver parenchyma. In
Masselis series[32], MRI accurately showed a local parenchymal invasion in 80% of the patients (Figure 12).

Figure 12 Arterial infiltration of cholangiocarcinoma. Multidetector computed tomography in the arterial phase shows a periductal mass in the hepatic
hilus completely surrounding the right hepatic artery consistent with tumor infiltration.

Recently, with the advent of functional imaging such

as positron emission tomography computed tomography
(PET-CT) that allows the study of the whole body, the
need for additional imaging in patients with cholangiocarcinoma has arisen, in order to rule out distant metastases before radical treatment. The utility of 18F-fluorodeoxyglucose (FDG) positron emission tomography
(PET scan) in the diagnosis and staging of HCCA is uncertain. Anderson et al[37] showed that PET can accurately
detect nodular cholangiocarcinomas as small as 1 cm with
a sensitivity of 85%. However, infiltrating tumors which
are more frequent are only detected in 18% of the cases.
The addition of PET-CT changed the initial management
in 30% of the cases by detecting unexpected distant metastasis. This study is relatively old and the results should
be interpreted cautiously, especially in patients with PSC
or biliary stents in place.
In a recent meta-analysis by Ruys et al [38], data of
the literature concerning diagnosis and staging of hilar
cholangiocarcinoma during the period 1966-2011 were
reviewed. The initial search yielded 766 articles but only
16 papers, which included 448 patients, met the inclusion
criteria and were actually analyzed. Most data concerned
CT as the primary diagnostic tool and therefore comparison with MRI and PET-CT was not possible. Only data
on CT were sufficient for pooling the findings. Pooled
accuracy of CT for assessment of ductal extent of the
tumor was 86%, whereas pooled sensitivity and specificity for assessment of portal vein involvement was 89%
and 92% respectively. Pooled sensitivity and specificity
in the assessment of hepatic artery tumoral involvement
was 84% and 93% respectively. Concerning regional
lymph node metastasis, pooled sensitivity and specificity
were 61% and 88%. Only one study that met the inclusion criteria reported the results of PET-CT for the assessment of lymph node metastasis with a sensitivity and
specificity of 42% and 80%, respectively[39].
Concerning distant metastases, the results of the meta-analysis are somewhat limited because only one study
reported on the sensitivity and specificity of incremental
non helical CT on metastasis (67% and 94% respectively).

Distant extension of cholangiocarcinoma: Distant

staging
Different imaging techniques are currently used for the
preoperative staging of hilar cholangiocarcinoma. However, accurate staging remains a challenge. Distant staging
is usually performed with CT or MR at the same time as
doing local vascular and biliary staging, yet most evidence
is available from CT. Although the quality of imaging has
improved in recent years, a substantial proportion of tumors are still found to be unresectable during laparotomy
despite extensive pre-operative work and only 50% of
the tumors surgically explored are eventually resectable[31].

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Valls C et al . Radiological diagnosis and staging of hilar cholangiocarcinoma

The same study reported a sensitivity and specificity of

56% and 88%, respectively for PET/CT in the detection
of distant metastasis. The series by Ruys et al[40] evaluated
retrospectively the additional value of FDG-PET/CT
in staging of hilar cholangiocarcinoma after extensive
conventional preoperative work-up with CT or MR.
The primary tumor was 18F-FDG-positive in 88% of
patients. However, all benign lesions in the series were
also FDG-positive. Sensitivity and specificity for the
detection of regional lymph node metastases and distant metastases were 67% and 68%, and 33% and 96%,
respectively.
To summarize, the data in the literature concerning
accuracy of imaging techniques in the diagnosis and staging of hilar cholangiocarcinoma are still very limited and
most studies have important methodological limitations
precluding direct head-to-head comparison of different
imaging modalities. The only evidence available concerns
staging with CT, which has acceptable accuracy for both
longitudinal and radial staging, with sensitivity and specificity ranging between 84% and 90%.
However, no solid evidence is available concerning
distant staging. The sensitivity of CT regarding lymph
node involvement seems to be low (61%) but this is
probably not very relevant in the planning of surgical
resection since lymphadenectomy is systematically performed in these patients. There are still no solid data
concerning the results of the different imaging modalities
in the distant staging of hilar cholangiocarcinoma.

8
9

10

11

12

13

14

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REFERENCES
1

5
6

Strom BL, Soloway RD, Rios-Dalenz JL, Rodriguez-Martinez

HA, West SL, Kinman JL, Polansky M, Berlin JA. Risk factors for gallbladder cancer. An international collaborative case-control study. Cancer 1995; 76: 1747-1756 [PMID:
8625043 DOI: 10.1002/1097-0142(19951115)76:10<1747::AIDCNCR2820761011>3.0.CO;2-L ]
Nakeeb A, Pitt HA, Sohn TA, Coleman J, Abrams RA, Piantadosi S, Hruban RH, Lillemoe KD, Yeo CJ, Cameron JL.
Cholangiocarcinoma. A spectrum of intrahepatic, perihilar,
and distal tumors. Ann Surg 1996; 224: 463-473; discussion
473-475 [PMID: 8857851 DOI: 10.1097/00000658-199610000-0
0005]
Klatskin G. Adenocarcinoma of the Hepatic Duct at Its Bifurcation Within the Porta Hepatis. An Unusual Tumor with
Distinctive Clinical and Pathological Features. Am J Med
1965; 38: 241-256 [PMID: 14256720 DOI: 10.1016/0002-9343(6
5)90178-6]
DeOliveira ML, Cunningham SC, Cameron JL, Kamangar
F, Winter JM, Lillemoe KD, Choti MA, Yeo CJ, Schulick RD.
Cholangiocarcinoma: thirty-one-year experience with 564
patients at a single institution. Ann Surg 2007; 245: 755-762
[PMID: 17457168 DOI: 10.1097/01.sla.0000251366.62632.d3]
Bosman FT, Carneiro F, Hruban RH, Theise N. WHO classification of tumours of the digestive system. 4th ed. Switzerland: WHO Press, 2012
Shin HR, Oh JK, Masuyer E, Curado MP, Bouvard V,
Fang YY, Wiangnon S, Sripa B, Hong ST. Epidemiology of
cholangiocarcinoma: an update focusing on risk factors.
Cancer Sci 2010; 101: 579-585 [PMID: 20085587 DOI: 10.1111/
j.1349-7006.2009.01458.x]
Burak K, Angulo P, Pasha TM, Egan K, Petz J, Lindor KD.
Incidence and risk factors for cholangiocarcinoma in primary

WJGO|www.wjgnet.com

16

17
18

19

20

21

22

23

125

sclerosing cholangitis. Am J Gastroenterol 2004; 99: 523-526

[PMID: 15056096 DOI: 10.1111/j.1572-0241.2004.04067.x]
Ben-Menachem T. Risk factors for cholangiocarcinoma. Eur
J Gastroenterol Hepatol 2007; 19: 615-617 [PMID: 17625428
DOI: 10.1097/MEG.0b013e328224b935]
Welzel TM, Graubard BI, El-Serag HB, Shaib YH, Hsing
AW, Davila JA, McGlynn KA. Risk factors for intrahepatic
and extrahepatic cholangiocarcinoma in the United States:
a population-based case-control study. Clin Gastroenterol
Hepatol 2007; 5: 1221-1228 [PMID: 17689296 DOI: 10.1016/
j.cgh.2007.05.020]
Wetter LA, Ring EJ, Pellegrini CA, Way LW. Differential
diagnosis of sclerosing cholangiocarcinomas of the common
hepatic duct (Klatskin tumors). Am J Surg 1991; 161: 57-62;
discussion 62-63 [PMID: 1846276 DOI: 10.1016/0002-9610(91)
90361-G]
Soto JA, Barish MA, Yucel EK, Siegenberg D, Ferrucci JT,
Chuttani R. Magnetic resonance cholangiography: comparison with endoscopic retrograde cholangiopancreatography.
Gastroenterology 1996; 110: 589-597 [PMID: 8566608 DOI:
10.1053/gast.1996.v110.pm8566608]
Fulcher AS, Turner MA. HASTE MR cholangiography in
the evaluation of hilar cholangiocarcinoma. AJR Am J Roentgenol 1997; 169: 1501-1505 [PMID: 9393153 DOI: 10.2214/
ajr.169.6.9393153]
Holzknecht N, Gauger J, Sackmann M, Thoeni RF, Schurig J,
Holl J, Weinzierl M, Helmberger T, Paumgartner G, Reiser M.
Breath-hold MR cholangiography with snapshot techniques:
prospective comparison with endoscopic retrograde cholangiography. Radiology 1998; 206: 657-664 [PMID: 9494483]
Yeh TS, Jan YY, Tseng JH, Chiu CT, Chen TC, Hwang TL,
Chen MF. Malignant perihilar biliary obstruction: magnetic
resonance cholangiopancreatographic findings. Am J Gastroenterol 2000; 95: 432-440 [PMID: 10685746 DOI: 10.1111/
j.1572-0241.2000.01763.x]
Tillich M, Mischinger HJ, Preisegger KH, Rabl H, Szolar
DH. Multiphasic helical CT in diagnosis and staging of hilar
cholangiocarcinoma. AJR Am J Roentgenol 1998; 171: 651-658
[PMID: 9725291 DOI: 10.2214/ajr.171.3.9725291]
Feydy A, Vilgrain V, Denys A, Sibert A, Belghiti J, Vullierme
MP, Menu Y. Helical CT assessment in hilar cholangiocarcinoma: correlation with surgical and pathologic findings.
AJR Am J Roentgenol 1999; 172: 73-77 [PMID: 9888743 DOI:
10.2214/ajr.172.1.9888743]
Nakanuma Y, Minato H, Kida T, Terada T. Pathology of
cholangiocellular carcinoma. Primary liver cancer in Japan
1994: 39-50
Lim JH. Cholangiocarcinoma: morphologic classification according to growth pattern and imaging findings. AJR Am J
Roentgenol 2003; 181: 819-827 [PMID: 12933488 DOI: 10.2214/
ajr.181.3.1810819]
Nakayama A, Imamura H, Shimada R, Miyagawa S, Makuuchi M, Kawasaki S. Proximal bile duct stricture disguised
as malignant neoplasm. Surgery 1999; 125: 514-521 [PMID:
10330940]
Binkley CE, Eckhauser FE, Colletti LM. Unusual causes
of benign biliary strictures with cholangiographic features
of cholangiocarcinoma. J Gastrointest Surg 2002; 6: 676-681
[PMID: 12399056 DOI: 10.1016/S1091-255X(01)00062-2]
Shanbhogue AK, Tirumani SH, Prasad SR, Fasih N, McInnes M. Benign biliary strictures: a current comprehensive
clinical and imaging review. AJR Am J Roentgenol 2011; 197:
W295-W306 [PMID: 21785056 DOI: 10.2214/AJR.10.6002]
Kloek JJ, van Delden OM, Erdogan D, ten Kate FJ, Rauws
EA, Busch OR, Gouma DJ, van Gulik TM. Differentiation
of malignant and benign proximal bile duct strictures: the
diagnostic dilemma. World J Gastroenterol 2008; 14: 5032-5038
[PMID: 18763286 DOI: 10.3748/wjg.14.5032]
Novotn I, Dt P, Trna J, Lata J, Husov L, Geryk E. Immunoglobulin G4-related cholangitis: a variant of IgG4-related
systemic disease. Dig Dis 2012; 30: 216-219 [PMID: 22722442

July 15, 2013|Volume 5|Issue 7|

Valls C et al . Radiological diagnosis and staging of hilar cholangiocarcinoma

33 Lee HY, Kim SH, Lee JM, Kim SW, Jang JY, Han JK, Choi BI.
Preoperative assessment of resectability of hepatic hilar cholangiocarcinoma: combined CT and cholangiography with
revised criteria. Radiology 2006; 239: 113-121 [PMID: 16467211
DOI: 10.1148/radiol.2383050419]
34 Cha JH, Han JK, Kim TK, Kim AY, Park SJ, Choi BI, Suh KS,
Kim SW, Han MC. Preoperative evaluation of Klatskin tumor: accuracy of spiral CT in determining vascular invasion
as a sign of unresectability. Abdom Imaging 2000; 25: 500-507
[PMID: 10931985 DOI: 10.1007/s002610000081]
35 Chryssou E, Guthrie JA, Ward J, Robinson PJ. Hilar cholangiocarcinoma: MR correlation with surgical and histological
findings. Clin Radiol 2010; 65: 781-788 [PMID: 20797463 DOI:
10.1016/j.crad.2010.04.018]
36 Ebata T, Nagino M, Kamiya J, Uesaka K, Nagasaka T,
Nimura Y. Hepatectomy with portal vein resection for hilar cholangiocarcinoma: audit of 52 consecutive cases. Ann
Surg 2003; 238: 720-727 [PMID: 14578735 DOI: 10.1097/01.
sla.0000094437.68038.a3]
37 Anderson CD, Rice MH, Pinson CW, Chapman WC, Chari
RS, Delbeke D. Fluorodeoxyglucose PET imaging in the
evaluation of gallbladder carcinoma and cholangiocarcinoma. J Gastrointest Surg 2004; 8: 90-97 [PMID: 14746840 DOI:
10.1016/j.gassur.2003.10.003]
38 Ruys AT, van Beem BE, Engelbrecht MR, Bipat S, Stoker J,
Van Gulik TM. Radiological staging in patients with hilar
cholangiocarcinoma: a systematic review and meta-analysis. Br J Radiol 2012; 85: 1255-1262 [PMID: 22919007 DOI:
10.1259/bjr/88405305]
39 Li J, Kuehl H, Grabellus F, Mller SP, Radunz S, Antoch G,
Nadalin S, Broelsch CE, Gerken G, Paul A, Kaiser GM. Preoperative assessment of hilar cholangiocarcinoma by dualmodality PET/CT. J Surg Oncol 2008; 98: 438-443 [PMID:
18767120 DOI: 10.1002/jso.21136]
40 Ruys AT, Bennink RJ, van Westreenen HL, Engelbrecht MR,
Busch OR, Gouma DJ, van Gulik TM. FDG-positron emission tomography/computed tomography and standardized
uptake value in the primary diagnosis and staging of hilar
cholangiocarcinoma. HPB (Oxford) 2011; 13: 256-262 [PMID:
21418131 DOI: 10.1111/j.1477-2574.2010.00280.x]

DOI: 10.1159/000336706]
24 Horger M, Lamprecht HG, Bares R, Spira D, Schmalzing
M, Claussen CD, Adam P. Systemic IgG4-related sclerosing
disease: spectrum of imaging findings and differential diagnosis. AJR Am J Roentgenol 2012; 199: W276-W282 [PMID:
22915418 DOI: 10.2214/AJR.11.8321]
25 Naitoh I, Nakazawa T, Ohara H, Ando T, Hayashi K, Tanaka H, Okumura F, Miyabe K, Yoshida M, Sano H, Takada
H, Joh T. Clinical significance of extrapancreatic lesions in
autoimmune pancreatitis. Pancreas 2010; 39: e1-e5 [PMID:
19924018 DOI: 10.1097/MPA.0b013e3181bd64a1]
26 Kamisawa T, Takuma K, Egawa N, Tsuruta K, Sasaki T.
Autoimmune pancreatitis and IgG4-related sclerosing disease. Nat Rev Gastroenterol Hepatol 2010; 7: 401-409 [PMID:
20548323 DOI: 10.1038/nrgastro.2010.81]
27 Lee YJ, Kim SH, Lee JY, Kim MA, Lee JM, Han JK, Choi BI.
Differential CT features of intraductal biliary metastasis and
double primary intraductal polypoid cholangiocarcinoma
in patients with a history of extrabiliary malignancy. AJR
Am J Roentgenol 2009; 193: 1061-1069 [PMID: 19770330 DOI:
10.2214/AJR.08.2089]
28 Diaz-Ruiz MJ, Falc J, Martin J, Bella RM, Carrasco M,
Tortajada L. Hepatocellular carcinoma presenting as portal
thrombosis with intrabiliary growth: US and MR findings.
Abdom Imaging 2000; 25: 263-265 [PMID: 10823447 DOI:
10.1007/s002610000029]
29 Toscano RL, Taylor PH, Peters J, Edgin R. Mirizzi syndrome.
Am Surg 1994; 60: 889-891 [PMID: 7978688]
30 Bismuth H, Castaing D, Traynor O. Resection or palliation: priority of surgery in the treatment of hilar cancer.
World J Surg 1988; 12: 39-47 [PMID: 2449769 DOI: 10.1007/
BF01658484]
31 Ito F, Cho CS, Rikkers LF, Weber SM. Hilar cholangiocarcinoma: current management. Ann Surg 2009; 250: 210-218
[PMID: 19638920 DOI: 10.1097/SLA.0b013e3181afe0ab]
32 Masselli G, Manfredi R, Vecchioli A, Gualdi G. MR imaging and MR cholangiopancreatography in the preoperative
evaluation of hilar cholangiocarcinoma: correlation with surgical and pathologic findings. Eur Radiol 2008; 18: 2213-2221
[PMID: 18463877 DOI: 10.1007/s00330-008-1004-z]

P- Reviewers Tougeron D, Sperti C S- Editor Huang XZ

L- Editor Roemmele A E- Editor Yan JL

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