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329© Springer International Publishing Switzerland 2016
J.M. Millis, J.B. Matthews (eds.), Diffi cult Decisions in Hepatobiliary
and Pancreatic Surgery, Diffi cult Decisions in Surgery: An Evidence-Based
Approach, DOI 10.1007/978-3-319-27365-5_29
Chapter 29
Assessment of Bile Duct Tumors: Endoscopic
vs Radiographic
Irving Waxman and Mariano Gonzalez-Haba
Abstract Cholangiocarcinoma (CCA) is the second most common primary liver
tumor and it’s associated with a poor prognosis. They diagnosis of CCA can be
challenging because of its paucicellular nature, anatomic location, and silent clinical character. Cross sectional radiologic studies (MRI/MRCP and multidetector CT
scan) are critical for diagnosis and staging CCA but their sensibility is yet improvable and they don’t allow tissue acquisition. ERCP has been for years the modality
of choice for evaluating and sampling biliary strictures for malignancy. New endoscopic techniques like EUS and cholangioscopy and advances in imaging technologies and cytology processing have the potential of signifi cantly improve the
preoperative diagnostic accuracy of this malignancy.
Keywords Cholangiocarcinoma • Diagnosis • Radiologic • MRI/MRCP • CT •
Endoscopy • Endoscopic ultrasound • ERCP
Introduction
Cholangiocarcinoma is the second most common primary liver tumor , after hepatocellular carcinoma ( HCC ), and it can arise anywhere in the biliary tree from the
intrahepatic ducts to the distal common bile duct at the ampulla of Vater . On the
basis of its location, cholangiocarcinoma can be divided into intrahepatic and extrahepatic tumors. Extrahepatic cholangiocarcinoma can be further subdivided into
perihilar (pCCA) and distal extrahepatic cholangiocarcinoma (dCCA). 20 % of all
CCA are intrahepatic, according to published series, whereas 50–60 % are perihilar,
up to 20 % are distal extrahepatic tumors and 5 % of tumors are multifocal [ 1 ].
Given the differences in their frequency, diagnosis and management , in this chapter
I. Waxman (*) • M. Gonzalez-Haba
Center for Endoscopic Research and Therapeutics (CERT), Center for Care and Discovery ,
The University of Chicago Medicine and Biological Sciences ,
5700 S Maryland Ave. MC 8043 , Chicago , IL 60637 , USA
e-mail:
iwaxman@medicine.bsd.uchicago.edu
330
we will comment separately intrahepatic, perihilar and distal extrahepatic
cholangiocarcinomas.
They diagnosis of CCA can be challenging because of its paucicellular nature,
anatomic location, and silent clinical character. A multidisciplinary approach that
involving radiographic, endoscopic , and biochemical analysis is often required.
Endoscopic retrograde cholangiography (ERC) with brush cytology and intraductal biopsy is the standard approach for diagnosis providing high specifi city, but
has proven limited diagnostic sensitivity. In this setting, Endoscopic ultrasound
(EUS) is increasingly used for CCA diagnosis and staging. Innovative imaging
technologies such as Intraductal Ultrasound (IDUS), cholangioscopy or advanced
cytologic techniques can improve the diagnostic yield of endoscopic procedures.
Patients with primary sclerosis cholangitis (PSC) deserve a special mention in this
chapter, as PSC is a major risk factor for developing CCA and its early diagnosis
can be particularly challenging.
A literature search of English language publications on PubMed/Medline from
2000 to 2014 was performed to identify published data on endoscopic and radiologic diagnosis on cholangiocarcinoma using the PICO outline (Table 29.1 ). Terms
used in the search were “cholangiocarcinoma” “ bile duct tumors” “cholangiocarcinoma AND diagnosis” “endoscopic diagnosis AND cholangiocarcinoma” “radiologic diagnosis AND cholangiocarcinoma” “EUS AND cholangiocarcinoma”
“ Primary sclerosing cholangitis AND cholangiocarcinoma”, “Cholangioscopy
AND cholangiocarcinoma” “EUS AND biliary stricture s,” “Endoscopic diagnosis
AND biliary strictures” 22 retrospective studies, 20 prospective studies, 5 guidelines, 3 systematic reviews, and 11 review articles were used. The data was classifi ed using the GRADE system.
Intrahepatic Cholangiocarcinoma (iCCA)
iCCA is often asymptomatic in early stages and can be an incidental fi nding on
cross-sectional imaging performed for other reasons. At more advanced stages, presentation can vary from constitutional syndrome to abdominal pain , jaundice , hepatomegaly, or a palpable abdominal mass. The diagnosis of intrahepatic
cholangiocarcinoma is basically radiologic , both MRI and CT scan can provide
accurate evaluation of tumor size and detection of satellite lesions. However, CT
may be better for assessment of vascular encasement, identifi cation of extrahepatic
metastasis and prediction of resectability [ 2 ]. Although imaging features of iCCA
Table 29.1 PICO table for endoscopic versus radiologic diagnosis of bile duct tumors
P (patients) I (intervention) C (comparator group) O ( outcomes measured)
Patients with
suspected bile duct
tumors
Endoscopic diagnosis Radiologic diagnosis
Yield of preoperative
diagnosis
Endoscopic/ radiologic
diagnosis
Post-surgical diagnosis
I. Waxman and M. Gonzalez-Haba
331
are often suggestive of the diagnosis, these criteria are insensitive for the diagnosis
of iCCA vs HCC in the presence of cirrhosis or from differentiating metastatic
adenocarcinoma and iCCA [ 3 ]. Pathological diagnosis is currently still required for
a defi nitive diagnosis of iCCA, especially in those patients who are poor candidates
for surgical resection [ 1 , 4 , 5 ].
Perihilar Cholangiocarcinoma (pCCA)
Patients with pCCA often present with symptoms of biliary obstruction and less
commonly cholangitis . Trans-abdominal ultrasonography can accurately localize
the level of obstruction as fi rst approach, but it has a very low yield for detection of
strictures or masses [ 6 ]. Cross sectional evaluation is critical for detection and eval-
uation of tumor extent . With the recent technical advances, overall accuracy of CT
for determining resectability of CCA is in the range of 60–85 % [ 2 , 6 – 8 ]. MRI
combined with MRCP is a noninvasive technique is emerging as an excellent tool
for evaluating ductal extension and for the preoperative assessment of biliary tract
cancers with accuracy up to 95 % [ 9 – 11 ]. However, MRI/ MRCP do not allow any
interventions to be performed, such as stent insertion, or tissue acquisition. If at all
possible, MRCP should be performed before biliary drainage since evaluation for
biliary pathology is more diffi cult if the biliary tree is collapsed from a preceding
biliary drainage [ 12 ]. The role of PET scan in the diagnostic algorithm of cholan-
giocarcinoma is evolving, although its utility for determining resectability of the
primary tumor is not superior to MRI/MRCP [ 13 ] but it might be a useful tool for
identifying occult metastases in patient’s a priori surgical candidates.
In an attempt to avoid unnecessary surgeries, staging laparoscopy was widely
performed to exclude local metastatic disease in suspected resectable patients; due
to improved imaging techniques its role will be probably limited in the upcoming
years [ 14 ].
Ca 19-9 is an established serum marker for cholangiocarcinoma , although its
sensitivity for the diagnosis is limited, in patients without PSC, serum Ca 19-9 values above 100 U/mL have a sensitivity of 53 % and specifi city of 75–90 % for the
diagnosis of CC [ 15 ]. CA 19-9 concentrations >1000 U/mL can predict advanced
disease and when elevated at diagnosis can be useful for follow up [ 16 ]. Importantly,
CA19-9 elevation frequently occurs in PSC and other causes of non-malignant
obstructive jaundice , but persistently raised levels of CA19-9 after decompression
suggest malignancy.
For years, ERCP has been the modality of choice for evaluating biliary stricture s
for malignancy. ERCP plays both a diagnostic and therapeutic role in the setting of
CCA as it has the power to evaluate the biliary tree and sample it via brush cytology
and endoscopic biopsy, but it can also provide means for biliary drainage or ablative
therapy, such as PDT or RFA . Brushings for cytology and biopsy samples for
histology can confi rm the diagnosis of CCA, however, the sensitivity of these tests
are limited, ranging from 18 to 60 % [
17 – 19 ]. This sensitivity can be raised by com-
29 Assessment of Bile Duct Tumors: Endoscopic vs Radiographic
332
bining tissue-sampling methods [ 20 – 22 ] and with the addition of newer diagnostic
tests, like fl uorescence in situ hybridization (FISH) and digital image analysis or
fl ow cytometry [ 23 – 25 ].
In this setting, EUS is becoming and emerging tool for the diagnosis and staging
of CCA, [ 16 , 19 , 26 , 27 ]. In a prospective evaluation of EUS-FNA on 44 patients
with hilar strictures suspicious of HC diagnosed by CT and/or ERCP , but with
inconclusive tissue, accuracy, sensitivity, and specifi city were 91 %, 89 %, and
100 %, respectively. Furthermore, EUS-FNA changed preplanned surgical approach
in 27/44 patients [ 16 ]. According to the largest single center recent study,
Mohamadnejad et al. reported a sensitivity of EUS-FNA for diagnosing CCA of
73 %, signifi cantly higher in distal than in proximal CCA (81 % vs. 59 %, respectively) [ 26 ]. EUS has also shown excellent specifi city for malignant biliary stric-
ture s but variable results in sensitivity in a recent metaanalysis and prospective
studies [ 28 – 31 ]. EUS can also have a great clinical value for the nodal staging in
extrahepatic CCA, as locoregional nodal metastasis will preclude liver transplant ation and distant nodal involvement can also contraindicate attempting a curative
resection . In a study performed by Gleeson et al. on 47 patients with CCA and
potential liver transplantation, preoperative EUS-FNA of regional lymph nodes was
performed in addition to their standard approach of exploratory laparotomy. EUS
identifi ed lymph nodes in all patients and 8/47 patients had positive lymphadenopathy confi rmed as malignant by pathologic examination. Based on these results,
17 % of their patients were spared the cost and morbidity of an unnecessary laparotomy. There were no morphologic criteria or echo features to correlate with nodal
malignancy. Furthermore, the EUS fi nding of absent regional lymph-node metastases was confi rmed in 20 of 22 by a subsequent exploratory staging laparotomy.
Interestingly, seven of these eight patients had PSC [ 32 ].
The possibility of tumor seeding during EUS-FNA in patients with suspected
extrahepatic CCA is a concern; especially for proximal bile duct lesions. It was
reported in a study on 191 patients with locally unresectable enrolled for neoadjuvant chemoradiotherapy followed by LT protocol, a total of 16 underwent transperitoneal FNA biopsy of the primary tumor (13 percutaneous and 3 EUS guided) [ 33 ].
It is important to note that percutaneous needle aspiration may carry a greater risk
of tumor seeding when compared to EUS-FNA [ 34 ]. Although these results have
not been reproduced in other studies [ 35 ] and until more data are available, tumor
seeding during EUS-FNA should be considered before performing a biopsy of a
potentially resectable proximal CCA.
Distal Cholangiocarcinoma
Distal biliary stricture s frequently present a challenge in terms of diagnosis , which
require a multidisciplinary approach. Often carcinomas arising within the area of
the major papilla of the duodenum are referred as periampullary carcinomas and
I. Waxman and M. Gonzalez-Haba
333
include the intrapancreatic distal bile duct , the head and uncinate process of the
pancreas and the duodenum. Their origins are often diffi cult to discern based on
clinical settings and results of preoperative imaging, as well as on surgical specimens [ 36 ]. CT scan and MRI / MRCP have similar outcomes to those in proximal
strictures, although MRI/MRCP can be superior to CT scan on differentiating
benign vs malignant strictures [ 11 , 36 ]. EUS has become the imaging test of choice
in patients with distal biliary obstruction , given its relative ease of visualizing and
sampling distal bile duct lesions with high sensitivity and accuracy for malignant
etiology, which is more frequently associated to pancreatic cancer . In the study of
Mohamadnejad, EUS-FNA allowed tissue diagnosis in distal tumors with 81 %,
compared to ERCP with brush cytology had only a 27 % sensitivity [ 26 ]. Given
higher incidence of pancreatic cancer compared with CCA, EUS-FNA should be
performed before ERCP in all patients with suspected distal malignant biliary
obstruction [ 37 ]. Combined EUS and ERCP can be performed in the same proce-
dure with no signifi cant impact on their separate outcomes or complications [ 38 ].
EUS might also have an important role in the diagnosis of early stage CCA. In a
recent study performed on 142 non icteric patients with an elevated alkaline phosphatase level and biliary dilation, MRCP followed by EUS was highly sensitive
(90 %) and specifi c (98 %) for the diagnosis of extrahepatic bile-duct carcinoma
[ 39 ].
Primary Sclerosing Cholangitis
Primary sclerosing cholangitis (PSC) is one of the best known risk factor for developing cholangiocarcinoma , with a 10-year cumulative incidence of approximately
7–9 % [ 40 , 41 ], furthermore, it is estimated that in as many as 50 % of patients with
CCA associated with PSC, this one is detected at the time of diagnosis or within the
fi rst year. Dominant strictures occurs in 45–58 % of patients during follow up [ 42 –
44 ] and should always raise the suspicion of the presence of a cholangiocarcinoma
(CCA). In patients with PSC, the distinction between a benign dominant stricture
and CCA can be challenging as because both benign and malignant strictures produce similar cholangiographic fi ndings. Patients with PSC and symptoms such as
cholangitis , jaundice , pruritus, right upper quadrant pain or worsening biochemical
indices should undergo endoscopic evaluation to rule out dominant strictures and
for associated therapy (likely biliary sphincterotomy and balloon dilatation with or
without stent placement). Before any attempt at endoscopic therapy, brush cytology
and/or endoscopic biopsies should be obtained to help exclude a superimposed
malignancy. According to recent meta-analysis, bile duct brushings for diagnosis of
CCA in patients with PSC were 43 % and 97 % respectively, with a raise in sensitivity up to 51 % when FISH polysomy was added [ 45 ].
In patients with PSC, Ca 19-9 level of 129 units/mL as a cut-off value found a
sensitivity, specifi city, positive predictive value, and negative predictive value of
29 Assessment of Bile Duct Tumors: Endoscopic vs Radiographic
334
78 %, 98 %, 56 % and 99 %, respectively in recent study on 208 [ 46 ]. Noteworthy,
in another study, more than one-third of patients with this cut-off level of CA 19-9
did not have cholangiocarcinoma after an average of 30 months of follow-up [ 47 ].
Cholangioscopy and intraductal US have also been used and are promising technologies for improving the diagnosis of CCA in PSC [ 48 , 49 ]. Currently there are
suggest an imaging study plus a CA 19-9 at annual intervals [ 1 , 50 ].
Novel Endoscopic Techniques
Peroral cholangioscopy is a technique for direct endoscopic visualization of the bile
duct s, allowing both for targeted tissue sampling and for intraductal interventions.
Cholangioscopy and visually targeted biopsies can improve the diagnostic accuracy
than standard ERCP [ 21 ]. Recent improvements in cholangioscopes with the advent
of single operator cholangioscopy system have led to a re-emergence of this technology [ 51 – 53 ]. The use of cholangioscopy with the current available technologies
is limited to patients in which other diagnostic tools have been attempted because of
potential adverse events and high equipment cost , as was shown in a recent study in
which EUS evaluation in patients with diffi cult biliary stricture prevented the need,
cost, and adverse events of cholangioscopy in 60 % of patients [ 54 ].
Intraductal ultrasound (IDUS) is based on the use of mini-probes (about 2 mm),
which can be passed through standard endoscopes directly into the bile or pancreatic duct. IDUS can overcome EUS limitations in the proximal biliary system and
surrounding vascular structures, improving its sensibility when compared to EUS
[ 55 – 57 ]. A recent study showed accuracy rates of 92 % of IDUS for the diagnosis
of CCA when compared with transpapillary biopsies (74 %) EUS (70 %) or CT scan
(79 %) [ 29 ].
Confocal laser endomicroscopy (CLE) is novel an imaging technique that provides real-time in vivo microscopic tissue examination during an ongoing endoscopic procedure, it has shown improvement for accuracy in diagnosis of
indeterminate pancreaticobiliary strictures in patients with and without PSC [ 19 , 58 ,
59 ]. Optical coherence tomography (OCT) uses infrared light refl ectance to produce
high-resolution cross-sectional tissue images through a probe, and has shown promising results in small studies [ 60 , 61 ]. These innovative techniques, with the poten-
tial of obtaining “true in vivo optical biopsies” are yet limited by their high costs,
lack of standardized criteria and insuffi cient prospective data on clinical outcomes .
Multicenter prospective trials are needed to further validate criteria and defi ne the
role of this technology compared with conventional tissue sampling techniques in
the diagnostic algorithm for indeterminate biliary stricture s.
I. Waxman and M. Gonzalez-Haba
335
Personal View
Cholangiocarcinoma is associated with a poor prognosis and can often pose a diagnostic challenge, especially in early stages due to diffi culties in obtaining an adequate specimen for cytology and the need to rule out benign conditions that can
mimic CCA in its early stages. Obtaining a tissue diagnosis is extremely important
in certain subgroups of patients such as those who are borderline surgical candidates, PSC patients with dominant strictures or before chemotherapy and radiation
therapy in patients non candidate for surgery . Cross sectional imaging like new
generation CT scan or especially MRI / MRCP can provide accurate data on resectability and tumor extension but with limited sensibility and no tissue acquisition.
ERCP has been for years the fi rst line approach for biliary stricture s owing to its
signifi cant diagnostic and therapeutic value when there is an additional need for
intervention and specimen acquisition power, but biliary brush cytology or forceps
biopsies have high specifi city with limited sensitivity. These limitations on CCA
diagnosis and staging have encouraged development of new technologies. Advances
in diagnostic methods like DIA and FISH can have increase the diagnostic yield of
brush cytology, but advantages are discrete and limited by price and local
availability.
Endoscopic ultrasound (EUS) provides accurate imaging for distinguishing
malignancy on indeterminate biliary obstruction , nodal staging for potentially
resectable tumors and enables tissue acquisition, however the risk of tumor seeding
along the needle tract after FNA has been reported. Despite a lack of prospective
data supporting this complication, it should be taken into consideration, especially
in patients potentially candidates for liver transplant ation , when deciding on a diagnostic approach for cholangiocarcinoma .
The combination of modern cross sectional imaging and endoscopic studies,
likely associating ERCP (with advanced cytology sampling) with EUS, and in experienced centers also nouvelle endoscopic techniques (such as cholangioscopy, IDUS
or confocal endomicroscopy) when necessary can minimize the proportion of
patients requiring diagnostic or staging surgery .
Recommendations
1. For intrahepatic cholangiocarcinoma , cross sectional imaging and tissue acquisi-
tion are required for diagnosis and staging. The role of endoscopy is limited in
this setting. (Evidence quality high; strong recommendation)
2. Patients with suspected extrahepatic cholangiocarcinoma should have
MRI / MRCP and CT scan as initial diagnosis for local and distant staging.
(Evidence quality high; strong recommendation)
29 Assessment of Bile Duct Tumors: Endoscopic vs Radiographic
336
3. ERCP should be performed when tissue diagnosis and/or when biliary drainage
is required. When available, advanced cytology techniques (FISH, DIA) should
be added (Evidence quality moderate, strong recommendation)
4. EUS should be considered for nodal staging of extrahepatic
cholangiocarcinoma .
The risk of seeding should be considered before performing FNA in patients
potentially candidates for curative surgery or biliary transplantation. (Evidence
of quality low, weak recommendation)
5. EUS should be the fi rst endoscopic modality for diagnosis , staging and tissue
acquisition on distal biliary obstruction (Evidence of quality moderate, weak
recommendation)
6. In indeterminate biliary obstruction s, EUS and ultimately advanced endoscopic
techniques (cholangioscopy, IDUS, pCLE…) should be attempted prior to surgical approach. (Evidence of quality moderate, weak recommendation)
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