Clinical News & Knowledge: Liver, Gallbladder & Biliary Tract Cancer
June 1, 2004
Oncology.
No. 7
Gallbladder and Biliary Tract Carcinoma: A Comprehensive Update, Part 1
VANDANA RAJAGOPALAN, MD
Fellow in Hematology/Oncology
St. Luke's-Roosevelt
Hospital Center and
Beth Israel Medical Center
WILLIAM P. DAINES
Harvard University
Boston, Massachusetts
MICHAEL L. GROSSBARD, MD
Chief of Hematology/Oncology
St. Luke's-Roosevelt
Hospital Center and
Beth Israel Medical Center
Associate Professor of
Clinical Medicine
Columbia University College of
Physicians and Surgeons
PETER KOZUCH, MD
Attending Physician
St. Luke's-Roosevelt Hospital Center
Assistant Professor of
Clinical Medicine
Columbia University College of
Physicians and Surgeons
New York, New York
Gallbladder carcinoma and carcinoma of the bile ducts are relatively
rare cancers in the United States. These cancers are often diagnosed
in an advanced stage due to their nonspecific symptomatology
and until recently have been associated with a dismal prognosis. Recent
advances in imaging and surgical techniques along with emerging
options in palliative chemotherapy have improved the outlook in
these cancers. While complete surgical resection remains the only hope
of cure in both these cancers, palliative biliary decompression and chemotherapy
result in substantial improvement in quality of life. Part 1 of
this review provides a relevant and comprehensive update of molecular
pathology, imaging modalities, and surgical care. In part 2, which will
appear next month, we will review palliative care and systemic therapy
in gallbladder and biliary tract carcinomas, as well as the use of liver
transplantation in the treatment of cholangiocarcinomas. These strategies
are of relevance to internists as well as oncologists caring for
these patients.
Gallbladder carcinoma and carcinoma
of the bile ducts are
relatively rare cancers in the
United States. Gallbladder cancer is
the more common biliary tumor in
this country, accounting for about
5,000 cases per year.[1] Until recently,
gallbladder cancer was associated
with a dismal prognosis. A better understanding
of the disease, its patterns
of spread, and its potential for cure
with radical surgery as well as advances
in various diagnostic tools have
led to improved survival in recent
years. Moreover, improvements in
palliative care including biliary decompression
techniques and chemotherapy
have expanded treatment options
for these diseases.
Cholangiocarcinoma, cancer of the
bile ducts, accounts for about 2,500
cases annually in the United States.[2,3]
Cholangiocarcinoma may be further
classified as intrahepatic or extrahepatic
(hilar and distal bile duct carcinomas).
The hilar tumors usually
require partial liver resection for cure,
whereas distal tumors may require
pancreatectomy. As with gallbladder
tumors, advances in diagnostic imaging
techniques permit earlier diagnosis
of these cancers and careful
selection of potentially resectable disease.
The search for appropriate neoadjuvant
or adjuvant treatments to
improve survival outcomes and decrease
recurrences is ongoing.
Part 1 of this two-part review summarizes
advances in preoperative imaging,
staging, and curative surgery.
In part 2, which will appear in next
month's issue, we will explore chemotherapy,
radiation therapy, and palliative
care, which are improving the
outlook for patients diagnosed with
these cancers.
Epidemiology
Gallbladder Cancer
Carcinoma of the gallbladder is a
rare malignancy generally associated
with a late presentation and a poor
prognosis. Nonmetastatic lesions carry
a 5-year survival rate of 32%, whereas
more advanced stages have a 1-year
survival rate of only 10%.[4] Affecting
1 to 2 people per 100,000, gallbladder
cancer is the fifth most common
cancer of the gastrointestinal tract in the
United States,[3] where between 2,000
and 5,000 cases of gallbladder cancer
are diagnosed each year.[1,3]
Incidence varies throughout the
world, with the most diagnoses and
highest mortality occuring in northern
India, northeastern Europe, and in
native populations in North and South
America. Mortality rates in these areas
can reach 5 to 10 times that in the
United States.[4] Western Native Americans
and Hispanic Americans are at an
increased risk compared to the general
US population, while African Americans
have been placed at equivalent or
slightly decreased risk compared to the
Caucasian population.[4,5] Increased
risk also is noted in women in Japan
and Israel.[6] The ratio of affected
women to men is variable according to
region, ranging between 1.5:1 and
6:1.[4,5,7] Risk increases with age, with
the maximum incidence occurring in
the 7th decade.[3]
- Risk Factors-Gallbladder carcinoma
has been linked to several risk
factors. Gallstones and chronic cholecystitis
commonly are associated with
the development of gallbladder cancer,
although neither is known to play
a strictly causative role.[6] Between
50% and 100% of patients diagnosed
with gallbladder cancer have concurrent
stones.[7] The incidence of neoplasm
in patients with gallstones and
no other risk factors or symptoms,
however, is very low (< 1%).[1,4] The
presence of larger gallstones may be
related to increased risk; patients with
gallstones larger than 3 cm are at 10
times the risk of patients with stones
smaller than 1 cm.[4,5] The incidence
of cancer in calcified (porcelain) gallbladder
has been estimated at 12.5%
to 61%.[6] Chronic inflammation of the
gallbladder, polyps, bacterial infections,
typhoid carrier status, ulcerative colitis,
and congenital anomalous pancreaticobiliary
duct junction also increase
risk.[5,6]
Although the imbalance of women
vs men suggests a role for hormonal
changes, disease pathogenesis studies
examining this role are inconclusive.[
5,6] Women with a history of
three or more pregnancies are at increased
risk. Late onset of menarche
and increased age at first childbirth
(> 20 vs < 20 years) has been observed
to decrease risk.[6,8]
The geographic distribution of disease
elicits continued investigation
into dietary and genetic risk factors.
High energy and high total carbohydrate
intake have been linked to gallbladder
cancer. The odds ratio
associated with high energy intake is
2.0, while the ratio associated with
total carbohydrate consumption is
11.3. A significant reduction in risk
has been associated with increased
vitamin B6 and vitamin E consumption.
Vitamin C, fat, and dietary fiber
intake have also been shown to provide
modest protection. High body
mass index is associated with a 2.1-
fold increase in risk in women, but
risk in men has not been observed to
relate to body mass index.[8]
Occupational exposures in the rubber,
automobile, wood-finishing, oil,
paper, chemical, textile, shoe, fiber
and metal-fabricating industries lead
to increased risk.[4,6] Likewise, both
tobacco chewing and smoking are associated
with increased risk.[6] The
consumption of carcinogenic impurities
in mustard oil may contribute to
elevated incidence in India.[5]
Cholangiocarcinoma
Cholangiocarcinoma-epithelial
cancer of the cholangiocytes lining
the biliary ducts-like gallbladder
cancer, generally presents late and allows
few options for curative intervention.
Incidence estimates range
from 0.8 to 2 per 100,000, with an
estimated 2,500 to 4,000 new cases
diagnosed each year in the United
States.[2,3,7] Several recent studies
indicate that the number of diagnoses
of cholangiocarcinoma is increasing
in the United States, United Kingdom,
and Australia.[2] Some of this increase
may be attributable to new methods
of diagnosis for obstructive jaundice
that identify extrahepatic malignancies
that previously would have been
misdiagnosed.[9] Incidence peaks in
the 8th decade of life[9] and is slightly
higher in men than in women.[10]
- Risk Factors-Risk factors for
cholangiocarcinoma are well understood,
although most patients lack
identifiable risks.[2] Patients with primary
sclerosing cholangitis carry an
elevated risk for cholangiocarcinoma
of 1.5% per year from onset of disease
and a lifetime risk of about
10%.[1,3] They usually present with
multifocal and unresectable carcinomas.[
3] Congenital choledochal cysts
increase the risk of cancer, most likely
due to associated inflammation and
bacterial infection. While early removal
of cysts lowers the likelihood of
malignancy, 15% to 20% of patients
with unexcised cysts or cysts treated
by bypass will develop cancer.[3]
Chronic ulcerative colitis, liver infection,
exposure to carcinogens (including
thorium dioxide, asbestos,
radon, dioxin, nitrosamines, and cigarette
smoke), and chronic intrahepatic
lithiasis are associated with
increased risk of cholangiocarcinoma.[
2,7] Approximately 2% of patients
with hepatitis C develop
cholangiocarcinoma,[7] and biliary
parasites such as Opisthorchis viverrini
and Clonorchis senensis contribute
to increased risk, especially in
Southeast Asia, where incidence can
reach 87 per 100,000.[3]
Patients can present with cholangiocarcinoma
in the intrahepatic, extrahepatic,
or hilar regions of the
biliary tract and generally do not survive
for more than 6 months after
diagnosis. The frequency of intrahepatic
tumors ranges between 10% and
33%, whereas the frequency of extrahepatic
and hilar cancers is 60% to
90%.[2,9] Less than 10% of patients
have diffuse or multifocal tumors.[9]
From 40% to 60% are perihilar and
proximal to the cystic duct and usually
require partial hepatic resection.[11]
From 20% to 30% are distal to the
cystic duct and are best treated with
pancreaticoduodenectomy.[11]
Pathology
Gallbladder Carcinoma
Most gallbladder cancers (99%) are
adenocarcinomas.[12] Infrequently,
tumors of the gallbladder can be of
mesenchymal origin-leiomyosarcoma,
rhabdomyosarcoma, or, more
rarely, carcinosarcoma, small-cell carcinoma,
carcinoid tumor, lymphoma,
or melanoma. Gallbladder tumors can
also be classified by their gross configuration
as infiltrative (causing thickening
and induration of the gallbladder),
nodular, and papillary, which has the
most favorable prognosis because of its
minimal invasive quality.[13] Infiltrative
tumors often present like a chronically
inflamed gallbladder, and the
tumors frequently are diagnosed only
after cholecystectomy.
Because of the proximity of the
gallbladder to segments IVb and V of
the liver, direct invasion by tumor
occurs often. Gallbladder cancer metastases
are common, with the incidence
of lymphatic and hematogenous
invasion reported in one study as 94%
and 65%, respectively.[14] Cancer
typically spreads around the bile duct,
to the cystic and pericholedochal
nodes. Later spread goes to portacaval
and celiac nodes, then to retropancreatic,
aortocaval, and superior
mesenteric artery lymph nodes.[3,5]
Direct invasion of the adjacent structures
such as duodenum, colon, anterior
abdominal wall, and common
hepatic ducts is extremely common.
More distant metastases to the lung
and brain have been observed in 32%
and 5% of patients, respectively.[15]
While knowledge of the molecular
pathology of gallbladder cancer is limited,
researchers have investigated the
role of ras, TP53 (alias p53), and
p16/CDKN2 abnormalities in gallbladder
cancer pathogenesis.[4] Small
studies report codon 12 K-ras mutations
in 0% to 59% of patients and
CDKN2 abnormalities in approximately
half of all patients. Molecular
pathogenesis is still unclear, although
evidence seems to point toward an
early and important role for p53 in
the development of malignancy.
Table 1 shows the commonly used
TNM systems for staging of gallbladder
cancer.[16,17]
Cholangiocarcinoma
Similar to gallbladder tumors, 90%
of cholangiocarcinomas are adenocarcinomas
and can be divided into
sclerosing, nodular, and papillary subtypes.[
18] Papillary tumors have been
associated with improved outcomes in
some retrospective analyses.[3]
Although the etiology of this neoplasm
is unknown, considerable
evidence points toward chronic inflammation
as a source of malignant
alterations. Proinflammatory cytokines
contribute to the overexpression
of nitric oxide synthase, which
produces chemicals promoting mutagenesis
and encouraging cell growth.
Bile acids are believed to transactivate
epidermal growth factor receptor
and induce cyclooxygenase (COX)-2
expression, which in turn inhibits
apoptosis and encourages cellular and
vascular growth. Allelic loss of p53
and bcl-2 has been observed in 30%
to 40% of tumors, while activation of
the oncogenes K-ras (50%-75%),
c-myc (95%), c-neu, c-erb-B2(0%-
73%), and c-met, as well as receptor
tyrosine kinases, COX-2, and human
aspartyl (asparaginyl) beta-hydroxylase
also have been observed in
limited series.[19] Disruptions of the
p14/MDM/p53 signaling pathway and
the retinoblastoma/p16/cyclin-dependent
kinase 4 cell regulatory pathway
have been found in both cholangiocarcinoma
and primary sclerosing
cholangitis, suggesting a common etiology
or a causative role for the inflammatory
condition.[19]
Cholangiocarcinoma metastasizes
readily to the liver, pancreas, hepatic
portal vein, hepatic artery, and lymphatic
systems. The incidence of
spread to the liver or peritoneum has
been reported to approach 50%, while
spread to regional lymph nodes is observed
in 75% to 80% of cases.[20]
Table 2 shows the TNM system used
to stage cholangiocarcinoma.[16]
Clinical Presentation
The symptoms related to gallbladder
carcinoma and cholangiocarcinoma
are relatively nonspecific, which
in part accounts for the often delayed
diagnosis. With a high index of suspicion
and the advent of better imaging
techniques, a preoperative diagnosis
of gallbladder carcinoma may be
reached in 75% to 88% of cases.[21]
The presentation of gallbladder or
cholangiocarcinomas can be divided
into five syndromes[22]:
(1) Acute cholecystitis: About 5%
of patients operated upon for acute
cholecystitis have occult gallbladder
neoplasms. An incidence of 6% to
8% has been reported in elderly patients
with acute cholecystitis, especially
when associated with abnormal
liver enzymes.[23] Therefore, it may
be reasonable to consider offering patients
with abnormal liver function
tests an open cholecystectomy instead
of a laparoscopic procedure.[24]
(2) Chronic cholecystitis: Recurrent
cholecystitis in a patient over age
50 with known gallstone disease
should raise suspicion for gallbladder
cancer.[25]
(3) Biliary tract disease: Symptoms
of biliary obstruction such as jaundice,
right upper quadrant pain, nausea,
vomiting, and in later stages,
pruritus are often associated with unresectable
disease. Mirizzi syndrome-
obstructive jaundice due to compression
of the common hepatic duct by an impacted
stone in the gallbladder neck-
has been associated with a high
incidence of gallbladder cancer, and in
such circumstances, intraoperative frozen
section is recommended.[26]
(4) Nonspecific symptomatology:
Anorexia, weight loss, and generalized
weakness are common symptoms
related to gallbladder cancer. Symptoms
can also result from local complications
such as fistula formation,
invasion of an adjacent organ presenting
with hemobilia, gastrointestinal
bleeding, or intestinal obstruction.
The presence of a palpable right upper
quadrant mass indicates unresectability
in most cases of gallbladder
carcinoma.[27]
(5) Symptoms and signs related to
metastatic disease
Patients with gallbladder cancer
can present with ascites, hepatomegaly,
and paraneoplastic syndromes such
as acanthosis nigricans. Most of these
symptoms can be caused by gallstone
disease alone.
Diagnostic Evaluation
Imaging studies guide preoperative
diagnosis, determine stage, and
help assess resectability (Table 3).
Multiple discontiguous liver metastasis,
ascites, peritoneal metastasis, distant
metastasis, extensive involvement
of the hepatoduodenal ligament, encasement
or occlusion of major vessels,
biliary involvement not amenable
to reconstruction, and poor performance
status are indications of
unresectable disease.[5] Direct involvement
of duodenum, liver, or colon
is not a contraindication to surgery.
Laparoscopy
Laparoscopic staging should be
considered prior to laparotomy in potentially
resectable disease because of
high rates of occult metastatic disease.
The overall accuracy of laparoscopy
in detecting unresectable disease
is 50% to 56%, which is more the
result of detecting peritoneal metastasis
than for locally advanced disease.[
28,29] If the patient has
radiologically unresectable disease,
pathologic diagnosis can be obtained
by needle biopsy to proceed with palliative
therapy.
Ultrasonography
Ultrasonography is the most common
radiologic study used to assess
gallbladder disease. Findings suggestive
of gallbladder cancer are discontinuous
gallbladder mucosa, mural
thickening, mural calcifications, a
mass protruding into the lumen, a
fixed mass in the gallbladder, loss of
the interface between the gallbladder
and the liver, or direct liver infiltration.[
30] All gallbladder polyps larger
than 1 cm, sessile polyps, and those
with eroded mucosa are suspicious
for carcinoma and should be resected.[
31-33] Duplex and B-mode ultrasonography
may be able to delineate
biliary, vascular, or nodal involvement,
but the sensitivity is only around
50%.[34,35]
Ultrasonography can evaluate potential
cholangiocarcinomas by revealing
dilatation of intrahepatic and/or
extrahepatic ducts, which in the absence
of gallstones and in the presence
of any discrete narrowing is
extremely suggestive of an obstructing
malignancy.[36] The diagnostic
accuracy of ultrasonography for cholangiocarcinoma
is limited in the setting
of primary sclerosing cholangitis
or cirrhosis.
Endoscopic ultrasound may be useful
in predicting the depth of tumor
involvement, defining the lymph nodal
involvement at the porta hepatic or
peripancreatic region, and obtaining
biliary cytology.[35,37] Endoscopic
ultrasound-guided fine-needle aspiration
is safe and effective in providing
a definitive diagnosis of gallbladder
and biliary tract carcinomas.[38,39]
Computed Tomography
Computed tomography (CT) scans
are inferior to ultrasonography in the
detection or evaluation of primary
gallbladder tumors but are more useful
in determining resectability by better
assessing extent of disease.[40]
Helical CT scans can predict resectability
with 93.3% accuracy.[41] CT
scanning is a poor modality for evaluation
of contiguous spread of gallbladder
cancer and detection of
omental spread.[42,43] CT scans are
sensitive in the detection of intrahepatic
bile duct carcinomas[44] but
limited in predicting resectability of
cholangiocarcinoma, with accuracy
ranging from 60% to 70%.[45]
Other Diagnostic Tools
Endoscopic retrograde cholangiopancreatography
(ERCP) and percutaneous
transhepatic cholangiography
(PTC) are useful in obtaining biliary
cytology for diagnosis. Biliary cytology
may be positive in about 75%
cases of gallbladder cancer, but the
procedure involves the risk of biliary
contamination, cholangitis, and sepsis.
ERCP and PTC are often used as
therapeutic measures to relieve biliary
obstruction by placement of a
stent. Noninvasive procedures such
as magnetic resonance imaging (MRI)
and magnetic resonance cholangiopancreatography
(MRCP) have generally
replaced these procedures, as
they better define resectability.[46]
MRI with MRCP is effective in
preoperative evaluation of gallbladder
carcinoma and cholangiocarcinoma.[
46,47] The sensitivity of MRI
and MRCP in studies has ranged from
67% to 100% for direct liver invasion
and 56% to 92% for lymph node
metastasis.[46,48]
Elevated carcinoembryonic antigen
(CEA) and CA19-9 in the presence of
biliary obstruction and nonspecific
symptoms raises the suspicion of gallbladder
cancer, but the sensitivity of
CEA is only 50% and that of CA19-9
is approximately 80%.[49,50]
We would like to acknowledge
Dr. Warren Enker, chief of
colorectal surgery at Beth Israel Medical Center
and professor of surgery at the Albert
Einstein College of Medicine in New York, and
Dr. Ronald Chamberlain, chief of hepatobiliary
and pancreatic surgery at Beth Israel and assistant
professor of surgery at the Albert
Einstein College of Medicine, for their critical
review of this manuscript
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