European Journal of Surgical Oncology 2000; 26: 438–443
doi:10.1053/ejso.1999.0918, available online at http://www.idealibrary.com on
Radical surgery for gallbladder cancer: current options
A. Muratore, R. Polastri and L. Capussotti
1° Department of Surgery, Ospedale Mauriziano ‘Umberto I’, Torino, Italy
Gallbladder carcinoma is the most common malignancy of the biliary tract. There are still many controversies regarding
the type of curative surgical treatment for each stage of the disease.
The staging system used is the TNM classification of the International Union Against Cancer. Different patterns
of spread characterize gallbladder cancer but the two main types are direct invasion and lymph node metastases;
since only the depth of invasion can be easily recognized by imaging techniques, it becomes the main variable in
choosing the appropriate surgical treatment. Most Tis and T1 tumours are incidentally discovered after cholecystectomy
for cholelithiasis and no further therapy is requested; for pT1b tumours, relaparotomy with hepatic resection and
N1 dissection is associated with a better survival. For T2 tumours, cholecystectomy with hepatic resection and
dissection of N1–2 lymph nodes is the standard treatment, with a 5-year survival of 60–80%. The only chance of
long-term survival for patients with a T3–T4 tumour is an extended operation combining an hepatic resection with
an N1–2 dissection with or without excision of the common bile duct. A subset of patients with peripancreatic
positive nodes or invasion of adjacent organs seems to benefit from a synchronous pancreaticoduodenectomy.
 2000 Harcourt Publishers Ltd
Key words: gallbladder; surgery; treatment; laparoscopy; lymph nodes.
Introduction
Carcinoma of the gallbladder was described for the first
time by Maximilian Destoll in 1777 but the first liver
resection for this disease was performed by Keen in 1881.1,2
More than 80% of gallbladder cancers are adenocarcinomas;
this malignancy is the most common of the biliary tract
and represented approximately 8.4% of the estimated cases
of liver and biliary tract cancers diagnosed in the USA
during 1994–1995.3
Carcinoma of the gallbladder is an aggressive and late
symptomatic disease and most patients are treated at an
advanced stage with a poor prognosis. During recent years,
extended operations combining a resection of the liver with
wide lymph node dissection have improved the long-term
survival.5,6 However, there are still many controversies
regarding the type of surgical treatment for each stage of
the disease.3,4,7
Staging system
The old classification of Nevin has been used for many
years;8 there are five stages defined according to the parietal
extension of the tumour: Stage I: intramucosa only; Stage
II: mucosa and muscularis; Stage III: mucosa, muscularis
Correspondence to: Andrea Muratore, V. Nizza 39, 10100
Torino (TO), Italy. Tel: +44 (0) 141-910124; E-mail:
[email protected]
0748–7983/00/050438+06 $35.00/0
and subserosa; Stage IV: cystic lymph node plus all three
layers; Stage V: liver by direct infiltration or metastases (to
the liver or any other organ). The most used staging system
for gallbladder carcinoma is the TNM classification of the
International Union Against Cancer (UICC)9 (Table 1).
Pattern of spread
Cancer of the gallbladder is characterized by diﬀerent
patterns of spread; an accurate knowledge of them is
important for determining the most rational surgical
treatment:
(1) Direct invasion of adjacent organs is a common mode
of spread: in terms of frequency, about 60% of the patients
have infiltration of the liver, followed by the colon, bile
duct, duodenum and pancreas.10 Macroscopically, there are
two patterns of hepatic invasion (Fig. 1): liver-bed type, in
which the tumour extends directly into segment IV–V from
the liver bed; and hilum-type, in which the cancer tends to
extend toward the hilum and to invade deeply into the liver
along Glisson’s sheat.1 When the type of invasion is studied
histologically, most liver-bed carcinomas have an expansive
spread, whereas most of the hilum type carcinomas have an
infiltrative spread.2,13 The knowledge of these two diﬀerent
patterns of infiltration is clinically important for determining
the resection procedure: resection of segment IVb–V in
patients with liver-bed type carcinoma achieves a high rate
of negative margins and seems associated to a better survival
than wedge resection; in the hilum type, extended right
 2000 Harcourt Publishers Ltd
Radical surgery for gallbladder cancer
439
Table 1. TNM classification of gallbladder cancer9
T-Primary Tumour
Tx primary tumour can not be assessed
T0 no evidence of primary tumour
Tis carcinoma in situ
T1 tumour invades lamina propria (T1a) or muscle layer (T1b)
T2 tumour invades perimuscular connective tissue without extension beyond serosa or into liver
T3 tumour perforates serosa (visceral peritoneum) or directly invades into one adjacent organ or both (extension into the liver Ζ2 cm)
T4 tumour extends >2 cm into the liver and/or into two or more adjacent organs (stomach, duodenum, colon, pancreas, omentum,
extrahepatic bile ducts, any involvement of liver)
N-Regional Lymph Nodes
Nx regional lymph nodes can not be assessed
N0 no regional lymph node metastasis
N1 metastasis in cystic duct, pericholedochal and/or hilar lymph nodes (hepatoduodenal ligament)
N2 metastasis in peripancreatic (head only), periduodenal, periportal, common hepatic artery, coeliac and/or superior mesenteric artery
lymph nodes
M-Distant metastasis
Mx distant metastasis can not be assessed
M0 no distant metastasis
M1 distant metastasis
Stage Grouping
Stage 0
Stage I
Stage II
Stage III
Stage IVA
Stage IVB
Tis
T1
T2
T1–2
T3
T4
Tany
Tany
N0
N0
N0
N1
N0–1
N0–1
N2
Nany
M0
M0
M0
M0
M0
M0
M0
M1
Fig. 1. Type of liver invasion in gallbladder cancer. A: liver-bed
type; B: hilum type.
hepatectomy achieves a higher rate of negative margins than
resection of segment IVb–V, but the type of resection does
not seem to improve the survival.12
(2) Many studies have stressed the significance of
haematogenous hepatic spread by a variable number of
small veins of the gallbladder draining directly into the
segment IV inferior and V via the liver bed.14–16 Instead,
this mode of spread seems to play a minor role in the early
phase of hepatic invasion; lymphatic spread, even in the
absence of direct hepatic infiltration, seems to be the main
method of diﬀusion through the liver.17 The rate of liver
metastases is about 10% in the absence of hepatic infiltration
and increases to 20% in presence of hepatic infiltration.12
According to these findings, wedge resection of the
gallbladder bed or resection of segment IVb–V has been
advocated by some authors for patients with T1b and T2
tumours.16,18,19
(3) Lymph node metastases are a common finding in
gallbladder carcinoma. Lymphatic drainage from the
gallbladder is along three main routes.20,21 The right route
is the main pathway: the lymph runs in the right half of
the hepatoduodenal ligament, along the nodes of the first
station (cystic, pericholedochal and proper hepatic artery
nodes), into the superior retropancreaticoduodenal or
retroportal nodes (second station) and, finally, into the paraaortic nodes (third station). The left route is a less important
way of lymphatic drainage: the lymph from the gallbladder,
after having reached the nodes of the first and second
stations, flows toward lymph nodes medial to the
hepatoduodenal ligament (anterior common hepatic artery,
posterior common hepatic artery, celiac trunk and superior
mesenteric artery nodes). Both right and left routes meet at
the lymph nodes around the pancreatic head. The third
route is the hilar route: the lymphatic drainage is toward
the hepatic hilus.
The overall rate of lymph node metastases ranges from
54% to 64%.19,21,22 The extent of the lymph node involvement
is strongly correlated with the depth of invasion of the
gallbladder carcinoma: a multicentre Japanese study has
shown that the rate of lymph node metastases is only 2.5%
in pT1a tumours, but it increases to 15.6% in pT1b tumours,
to 44.3% in pT2 tumours and to 72% in pT3–4 tumours.18
The pericholedochal lymph node is the most common
metastatic node followed by the cystic, posterosuperior
pancreaticoduodenal, retroportal, common hepatic artery
and celiac trunk nodes (Table 2). Moreover, pT3–4 tumours
have a higher N2:N1 ratio than pT2 tumours.5,22
(4) Intraductal spread of gallbladder carcinoma is
440
A. Muratore et al.
Table 2. Rate of lymph node involvement in patients with
gallbladder carcinoma21,22
Site
Group
Cystic lymph node
Pericholedochal lymph node
Proper hepatic artery lymph node
Retroportal lymph node (cephalad)
Retroportal lymph node (caudad)
Posterosuperior pancreaticoduodenal
lymph node
Common hepatic artery lymph node
Celiac trunk lymph node
Posteroinferior pancreaticoduodenal
lymph node
Superior mesenteric artery lymph node
Interaorticocaval lymph node
Frequency
N1
N1
N1
N1
N2
N2
25%
32%
10%
4%
20%
20–35%
N2
N2
N2
20%
15%
3%
N2
M1
10%
19–25%
characteristic of the papillary tumours: the tendency for
this histological subtype to grow intraluminally seems to
explain the more favourable prognosis.22
Treatment
The depth of tumour invasion and the presence of metastatic
lymph nodes are the main prognostic factors; however, only
the T factor can be easily recognized by pre-operative
imaging techniques or intraoperative ultrasonography, and
it becomes a useful variable for choosing the most
appropriate surgical treatment. Whatever the extension of
the resection, the achievement of a negative margin is
mandatory for long-term survival: the rate of histological
curative resection (R0) is 100% for stage I–II tumours and
48–52% for stage III–IV tumours.5,23
Tis-1 tumours
Tis and T1 tumours are usually pathological findings after
laparoscopic cholecystectomy for cholethiasis; Tis and T1
lesions are found respectively in 4% and 15–40% of patients
resected for gallbladder cancer.5,18,24,25
For pTis and pT1a tumours, cholecystectomy alone oﬀers
the greatest probability of cure with low morbidity and
mortality rates: the 5-year survivals range from 83% to
100%.16,26–28 Simple cholecystectomy, as adequate treatment
for pT1b patients, is still a matter of discussion; Shirai has
reported a favourable outcome regardless of the operation
done, cholecystectomy alone or extended cholecystectomy,
in a group of 11 patients with the tumour invading the
muscle layer.26 The results reported by other authors after
simple cholecystectomy for pT1b cancer are not as good,
with a 5-year survival ranging from 40% to 50%;16,28 Benoist
has recently reported the findings of a multicentre
retrospective study: of 23 patients with pT1b tumours who
underwent cholecystectomy alone, six died of recurrence,
whereas, of 13 with pT1a cancers, only one died of
recurrence.25 Moreover, another multicentre study has
reported a 5-year survival of 18% for 20 pT1 patients treated
by cholecystectomy alone.27 The 5-year survival for the
subset of pT1b patients increases to 72–100% after a more
extended procedure (cholecystectomy with hepatic resection
and lymph node dissection).5,15,18,21,28 These results are
supported by the findings of a recent multicentre Japanese
study of 1686 patients resected for gallbladder cancer: the
rate of lymph node metastases was 2.5% in 201 patients
with a pT1a tumour but increased to 15.5% in 165 patients
with pT1b tumours.18
In conclusion, most of the Tis and T1 tumours are an
incidental discovery after laparoscopic cholecystectomy for
gallstone disease: simple cholecystectomy is an adequate
treatment for patients with pTis or pT1a tumours and no
further reoperation is necessary; in the presence of
infiltration of the muscle layer (pT1b), cholecystectomy with
hepatic resection (wedge resection of the gallbladder bed or
segment IVb–V resection) and lymph node dissection (NI
station) seems to be associated with a better long-term
survival.
T2 tumours
The rate of metastatic lymph nodes ranges from 40%
to 60%, with a 20% rate of metastases to N2 lymph
nodes.5,18,22,21 Moreover, some studies have reported that,
even in the absence of hepatic infiltration, liver metastases
(mainly in the gallbladder bed) are possible.12,17 The 5-year
survival for patients with pT2 tumours is 22–40% after
simple cholecystectomy but increases to 60–80% after a
more extended resection.6,24,25,29,30 Indeed, cholecystectomy
with hepatic resection and dissection of N1–2 lymph nodes
is the standard treatment for patients with pT2 gallbladder
cancer; whether a wedge resection or a segment IVb–V
resection should be performed is unclear: no significant
benefits in terms of long-term survival have been
demonstrated by the use of either of these two procedures.12
Patients with a pT2 tumour discovered after a
laparoscopic cholecystectomy should undergo a radical
reresection: a recent study has shown the presence of
metastatic lymph nodes in 50% of reresected T2 patients.31
T3–4 tumours
The treatment of advanced gallbladder carcinomas is a
challenging problem, with a 5-year survival rate ranging
from 15% to 50% for pT3 tumours and from 7% to 25%
for pT4 tumours.18,19 The extent of hepatic resection is still
unclear: resection of segment IVb–V should be performed
for patients with liver-bed carcinoma; an extended right
hepatectomy seems the appropriate treatment to control
direct liver infiltration for hilum type carcinomas or liverbed carcinomas with an infiltrating pattern.11,12 The main
goal of hepatic resection is the achievement of a negative
margin which is the only chance of long-term survival.5,19,32
Since a high rate of lymph node involvement is common
for T3–4 carcinomas, dissection of N1 and N2 lymph nodes
is mandatory. Lymph node status is an important prognostic
factor and, despite the negative results of a multiinstitutional French study, long-term survival is possible;16,19,25 Tsukada has reported that, of 60 patients with
lymph node metastases, 11 with N1 spread and four with
N2 survived for more than 5-years.5 Indeed, metastases to
441
Radical surgery for gallbladder cancer
N1 or N2 lymph nodes discovered by frozen section are
not a contraindication to a curative resection.
Some
Japanese
authors
have
attempted
pancreaticoduodenectomy (PD) combined with hepatic
resection for patients with metastatic peripancreatic lymph
nodes (N2) or direct invasion of adjacent organs (T3–4), in
an eﬀort to improve the prognosis.18,33 In a recent study,
Shirai reported the results of 17 patients who had undergone
combined PD and hepatectomy for stage III or IV
carcinoma: of the five 5-year survivors, four had stage IVB
disease (N2 lymph nodes).32 However, this approach is
associated with a rate of post-operative complications
ranging from 34% to 70%.5,33,34
Many Japanese surgeons routinely performed resection
of the common bile duct in the course of a curative resection
for advanced gallbladder cancer because the lymphatics
surrounding the duct are a main route of tumour
spread;5,21,35 however, no improvement in long-term survival
has been reported as the result of this resection.36 Our and
other authors’ approach is the resection of the common bile
duct when, on gross examination, the tumour is close to or
infiltrates the bile duct (hilum type tumour).37 However, bile
duct involvement is associated with a higher rate of positive
margins, of metastases to para-aortic lymph nodes and with
a worse prognosis.11,20,23,32
The rate of para-aortic lymph node metastases ranges
from 19% to 25% in patients with locally advanced disease
but the value of para-aortic lymphadenectomy has not
been defined yet.21,22,37 All the authors but Yokoyama have
reported no long-term survivors among the patients with
metastases in this region;21,22,38 the latter author has examined
the incidence of lymph node micrometastases: of four
patients with positive para-aortic nodes, one was alive and
disease-free at 72 months. Therefore, lymphadenectomy of
this region may be reasonable for pT3–4 tumours and the
discovery by frozen section of a positive node does not
preclude a curative resection although the prognosis is poor
with very few long-term survivors.
Another controversial issue is the use of adjuvant
chemotherapy and radiotherapy after curative resection of
advanced gallbladder carcinomas: a recent report, at the
1999 ASCO Meeting, on 112 patients who had undergone
curative resection and were randomized to receive surgery
alone or surgery and chemotherapy has shown a significantly
better 5-year survival rate for patients receiving adjuvant
chemotherapy.39 However other studies are needed to
confirm these results. The aim of adjuvant radiotherapy is
to reduce the high rate of loco–regional failure after curative
resection: some authors have reported an improved survival
after adjuvant radiotherapy but each report was based on
a retrospective study with few cases.40–42 A recent study has
shown that adjuvant radiotherapy yielded a significantly
better 5-year survival rate than resection alone (17.2% vs
0%; P=0.0028) when radiation was used on patients with
microscopic cancer residues; however, no significant
improvement of survival time was detected using adjuvant
radiotherapy in patients with no cancer residues or with
macroscopic residues.43 Moreover, the rate of distant
metastases was not statistically diﬀerent between the
resection alone group and the adjuvant group. Therefore,
Gallbladder cancer
Post-operative diagnosis
Tis-1a
T1b T2
T3-4
Pre- or intraoperative
diagnosis
pTis-1a* pTis-1b* pT2-3-4
No further
therapy
Chole
Chole + WR +
N1
Type of reresection
depending on pT
Chole + WR or
IVb-V + N1-N2
Chole + IVb-V or EH + NI-N2
± VB or ± PD
Fig. 2. Algorithm for management of gallbladder cancer based on
depth of the tumour. Chole: cholecystectomy; WR: wedge resection;
IVb-V: resection of segment IVb-V; EH: extended right
hepatectomy; PD: pancreaticoduodenectomy; VB: resection of
common bile duct; N1: dissection of N1 lymph nodes; N2: dissection
of N2 lymph nodes; h>: optional treatment; ∗ usually pathological
findings, rare pre-operative diagnosis.
other studies are needed to evaluate the role of combined
radiotherapy and chemotherapy after curative resection.
In conclusion, patients with T3–4 tumours should
undergo resection of segment IVb–V (liver-bed type) or
extended right hepatectomy (hilum type or liver-bed type
with deep infiltration) associated to N1–2 dissection. In the
presence of a tumour close to or infiltrating the duct,
resection of the bile duct is mandatory. Combined PD and
hepatectomy can be an eﬃcacious treatment for selected
patients with stage III–IV tumours provided that a curative
resection can be performed with low morbidity and mortality
rates. Recent reports seem to suggest a role for radiotherapy
and chemotherapy after curative resection of advanced
gallbladder cancer.
Laparoscopy and port site recurrence
The incidence of port site recurrence of carcinoma after
laparoscopic procedure ranges from 8% to 19%;31,44,45 most,
but not all, such recurrences are at the site of gallbladder
removal.46,47 Many experimental studies have demonstrated
that
cellular
dissemination
during
laparoscopic
cholecystectomy is frequent and that pneumoperitoneum
significantly increases tumour implantation and growth at
trocar sites.48,49 Moreover, another recent experiment study
has reported that peritoneal injuries, i.e. caused by trocar
insertion, enhance peritoneal implantation of carcinoma
cells.50 Thus, if gallbladder cancer is diagnosed or suspected
pre-operatively, an open laparotomy is indicated; if it is
diagnosed during laparoscopy, the laparoscopic procedure
should be converted to an open procedure with excision of
port sites. Patients with a pT1b–4 tumour discovered on
the final pathology report need a reoperation with excision
of trocar port sites.31,46
442
A. Muratore et al.
Conclusions
The most appropriate surgical treatment of gallbladder
cancer is determined on the basis of the depth of infiltration
(Fig. 2). Most Tis or T1 tumours are discovered incidentally
after cholecystectomy: no further therapy is requested for
pTis or pT1a tumours whereas relaparotomy with wedge
resection and N1 dissection is necessary for pT1b.
Cholecystectomy with hepatic resection (wedge resection or
resection segment IVb–V) and N1–2 lymph node dissection
improves the long-term survival of patients with T2 tumours.
The only chance of long-term survival for patients with T3
or T4 gallbladder cancer is an extended operation combining
an hepatic resection (segment IVb–V or extended right
hepatectomy) with a N1–2 dissection, with or without
resection of the common bile duct. Pancreaticoduodenectomy combined with hepatic resection seems to
improve the survival in patients with metastatic
peripancreatic nodes or direct infiltration of adjacent organs,
provided that a curative resection can be obtained with low
morbidity and mortality rates. Moreover, recent reports
seem to suggest a role for radiotherapy and chemotherapy
after curative resection of advanced gallbladder cancer.
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World Wide Web Site Reviews
In order to help and to encourage our readers to make the best use of the cancer related and surgical oncology
resources on the Internet, we are pleased to oﬀer to publish short Web Site Reviews in the Highwayman series. A
review may address any site in the broad subject range of our remit or in relation to our recently published articles.
The site under review might be a search engine; an information or reference source, of historical or biogeographical
interest; a cancer charity; a grant giving body; a complementary or alternative medicine source; or oﬀbeat.
Kim et al. have recently published a series of criteria for evaluating health related web sites, which provide a useful
framework for would be reviewers. They include:
—the content of the site, including quality, reliability, accuracy, scope and depth;
—design and aesthetics, layout, interactivity, presentation, appeal, graphics and use of media;
—disclosure of authors, sponsors and developers;
—currency of information and maintenance of the site;
—the authority of the source;
—the ease of use, including facility to download, navigability and functionality;
—quality of links to other sites;
—attribution and documentation;
—appropriateness for intended audience;
—contact addresses and feedback mechanisms;
—user support;
—unique features.
Reviews should be between 200 and 500 words, and without illustrations or screen snapshots. They may be
submitted for publication either as signed reviews or anonymously under the ‘Highwayman’ imprint. They oﬀer a
particular opportunity for your trainees and younger web wizards to exercise their pens and keyboards in creative
writing.
Reference
1. Kim P, Eng TR, Deering MJ, Maxfield A. Published criteria for evaluating health related Web sites. BMJ 1999; 318: 647–9.