Tadashi Sagoh, MD #{149} Kyo Itoh, MD #{149} Kaori Togashi, Shunsuke Minami, MD #{149} Satoshi Noma, MD #{149} Keiji Reinin Asato, MD #{149} Keiichiro Mori, MD #{149} Toshikuni Yoshihisa Nakano, MD #{149} Junji Konishi, MD
Gallbladder Carcinoma: with MR Imaging’ Magnetic resonance (MR) images of 19 patients with histologically proved gallbladder carcinoma were retrospectively reviewed to determine the appearance of the primary tumor, and to assess the ability of MR imaging to demonstrate the various modes of tumor spread beyond the gallbladder. The primary tumor, as well as tumor spread beyond the gallbladder, was hyperintense on T2-weighted images and hypointense on Ti-weighted images when compared with the liver parenchyma. Liver invasion and metastasis could be depicted by MR imaging with both sequences, unless the tumors were small or the extent of invasion was minimal. Duodenal invasion was difficult to evaluate because of motion artifacts, paucity of fat, and partial volume effects. Tiweighted images readily demonstrated extension of the tumor to the hepatoduodenal ligament and paraaortic region with good contrast between tumor and surrounding tissue. The extent of tumor extension to the blood vessels was also easily evaluated because of flow void in the vasculature. MR imaging can help determine the extent of gallbladder carcinoma and can contribute to the staging of this disease. Index
terms:
762.1214 762.3212
Gallbladder,
#{149} Gallbladder,
MR studies, neoplasms,
762.321,
1990;
confined to the gallbladder, the tumon can be easily resected, but it usually is not detected until it reaches an advanced state that has extended beyond the gallbladder (1-4). Ultrasonognaphic (US) and cornputed tornographic (CT) findings in gallbladder carcinoma have been presented previously (5-11), and mecently, magnetic resonance (MR) irnaging has been reported to be a useful method in the evaluation of the biliany system (12-15). To our knowledge, however, theme are no consecutive MR studies of gallbladder carcinoma. The purpose of our study is to determine the MR findings of gallbladder carcinoma and to assess the ability of MR imaging to demonstrate its various modes of spread.
PATIENTS
1988. Within MR imaging, gery. In six
SM.,
SN.,
Department (T. Sagoh.
of Radiology and NuK.I., K.T., T. Shibata,
KY., K.N., R.A., Y.N., J.K.), the 5cc-
ond Department of Surgery (KM.), and the First Department of Surgery (TN.), Kyoto Univemsity School of Medicine, 54 Kawahama-cho, Shogoin, Sakyo-ku, Kyoto-shi, 606 Japan. From the 1988 RSNA annual meeting. Received Dccember 3, 1988; revision requested January 23, 1989; revision received August 30; accepted September 5. Address reprint requests to T. Sagoh. © RSNA. 1990
METHODS
1-2
weeks
after
all patients cases
the
portal
vein
found
beyond
tologic
diagnosis
patients. MR imaging
the
was
pan-
in 13 cases
procedures
At surgery, to have some
tension all
and
and
were
a
pen-
all patients were degree of tumor
cx-
gallbladder.
his-
adenocarcinoma
The
and
two
acquisitions
Images matrix matrix. tamed body were
used for SE 2,000/20, 60 sequences. were acquired ‘ ith a 256 X 256 and displayed with a 512 X 512 In all patients, images were obin the transverse plane with a coil. Spatial presatunation pulses used in seven cases, and in two of
these
cases,
respiratory
compensation
was
also used. Field of view was 29-34 cm depending on the patient’s size. MR findings of gallbladder carcinoma on
Ti-
and
T2-weighted
images
were
net-
nospectively analyzed to determine the appearance of primary tumor and its vanous modes of spread. These include direct liver invasion, distant liver metastasis, duodenal invasion, and extension to the hepatoduodenal ligament and paraaortic region. In all cases of direct liver or duodenal invasion,
operative
records
were
avail-
able, and MR findings were compared with surgical results. In cases of liven metastasis and tumor extension to the hepatoduodenal ligament and paraaortic negion, confirmation was limited, as these regions could not be examined completely even
at surgery.
To help assess the role in evaluating gallbladder compared
MR
results
of MR imaging carcinoma, we to CT
findings
available.
cx-
or lobectomy of of the hepatolymphatic dis-
resection,
of palliative
were
sequences
were
when
sun-
procedures
600/25
also
undergoing
underwent
tensive (wedge resection the liver, skeletonization duodenal ligament with
formed. From the clear Medicine I
AND
Nineteen patients with gallbladder carcinoma-six men and 13 women, aged 33-80 years (mean, 64.8 years)-wene studied with MR imaging at Kyoto University Hospital from June 1985 to May
variety
MD
weighted images was 2,000/20, 60. The section thickness was 5 mm, with intersection gaps of 2.5 on 5 mm. Four signal acquisitions were used for SE 600/20 on
RIMARY carcinoma of the gallbladder is an infrequent but rapidly progressive malignancy with a very high mortality rate (1,2). When
creaticoduodenectomy),
174:131-136
Nishimura,
Evaluation
P
section,
Radiology
MD #{149} Toshiya Shibata, MD Yamashita, MD #{149} Kazumasa Nishikawa, MD
in
was performed with a superconducting magnet operating at 1.5 T (Signa; GE Medical Systems, Milwaukee). Ti-weighted images were obtained by using spin-echo (SE) pulse sequences of 600/25 (repetition time [FR] msec/echo time [TE] msec) or 600/20. The pulse sequences for proton density and T2-
RESULTS In all patients, MR imaging showed the primary tumor of the gallbladder. The tumor exhibited two patterns. In 1 1 cases, the tumor showed the “massive” pattern seen as a large mass almost replacing the gallbladder on the gallbladder fossa (Figs 1-3). The “infiltrative” pattern showed focal on diffuse wall thickening and was present in eight cases (Figs 4, 5). No tumor appeared as a
Abbreviations: time,
TR
=
SE repetition
spin time.
echo,
TE
echo
131
a. Figure 1. Massive-type tumor with lucent 60) MR image, and (c) CT scan. A large mass heads, a and b) The mass is hypointense on (b) relative to the liver panenchyma. Stones arc difficult to identify on the CT scan (c).
on intraluminal mass. When compared with liven parenchyma, the primary tumor was slightly or definitely hypointense on Ti-weighted images and was slightly on definitely hyperintense with some inhomogeneity on T2-weighted images. When compared with sumrounding fatty tissue, the tumor was definitely hypointense on Ti-weighted images and was isointense or slightly hypenintense on T2-weighted images. In i 1 cases, gallstones were seen as signal defects sometimes trapped in the tumor (Figs 1, 3). In two cases, the stones were radiolucent and were difficult to identify on CT scans (Fig ic). Direct liver invasion was demonstrated on MR images in 1 1 cases as ill-defined tumor masses in the adjacent liven parenchyma contiguous to the primary gallbladder tumor (Figs 1-3, 5, 6) and was confirmed at sumgery in all cases. In two cases, howeven, minimal liven invasion found at surgery was not seen on MR images because of poor signal contrast between the tumor and the liver parenchyma in one case (Fig 7) and because of partial volume averaging in the other. In five cases, distant liver metastasis was depicted on MR images as multiple or solitary round nodules (Figs 8, 9). In all five cases, at least one of the nodules depicted at MR imaging was confirmed at surgery. In three of the 14 remaining cases, sungically proved metastatic nodules smaller than 2 cm were not seen at MR imaging. Because the entire liver parenchyma could not be examined at surgery, more lesions might have been missed. The signal intensity of tumor spread in direct liven invasion and distant liven metastasis was similar to
b. stones
c. invading
occupies
the
the liver
seen
gallbladder
the Ti-weighted image trapped in the mass are
on (a) Ti-weighted
fossa
and
(a) and clearly
directly
hyperintense identified
(600/25)
invades
and
the
more
as signal
MR image, adjacent
visible
defects
(b) T2-weighted
liver
parenchyma
on the T2-weighted
(arrow,
a and
b) on
(2,000/ (arrow-
image
MR
images
but
fungating
132 #{149} Radiology
a.
b.
Figure 2. Massive-type (a) Ti-weighted (600/20)
tumor
extending
MR images
tion were used) and ligament (arrowheads, Direct liven invasion
(b)
the hepatoduodcnal CT scan (b).
ligament
to the
(spatial
liver
and
presaturation
CT scan. Nodular and infiltrative a). Hepatic artery (curved arrow, (straight arrows, a) is also apparent.
and
its relation
a.
to surrounding
the
hepatoduodenal
pulses masses a) tumor Extension
ligament
respiratory
on
compensa-
invade the hepatoduodenal involvement is depicted. of the primary tumor
blood
vesels
are unclear
to
on the
b.
Figure
3. Massive-type tumor that extends to the liven and the on (a) Ti-weighted (600/25) and (b) T2-weighted (2,000/60) MR invading the liver and the hepatoduodenal ligament. Involvement (straight arrow, a) and hepatic artery (curved arrow, a) is depicted.
bile duct is also apparent arrow, b).
and
(arrowheads,
a and
b). Gallstone
hepatoduodenal
ligament
images. A large mass is seen of the portal vein Dilatation of intrahepatic
is trapped
within
the tumor
January
(open
1990
fat tissue duodenum contrast.
between because
the tumor of poor
and signal
the
In 15 cases, tumor extension to the hepatoduodenal ligament and paraaortic region was seen as nodular or infiltrative masses on Ti-weighted images (Figs 2-7). In iO of these cases, these regions were explored at surgery, and tumor spread to these areas was confirmed. In the other five cases, surgical exploration of these areas was not performed. In two cases surgically proved hepatoduodenal lymph node metastases were missed at MR imaging. In both
cases
a.
b.
Figure
4.
weighted extension
Infiltrative-type
tumor
with
extension
images. Fundus of the gallbladder to the hepatoduodcnal ligament
surrounding
the
portal
vein.
The
to the
hepatoduodenal
ligament
shows irregular wall thickening is identified as infiltrative masses
netnopancreatic
region
a.
is not
involved
on
Ti-
(arrow), and (arrowheads,
a)
(b).
b.
Figure 5. Infiltrative-type tumor extending to the liver and the hepatoduodenal ligament on (a) Ti-weighted (600/20) and (b) T2-weighted (2,000/60) MR images. Spatial pnesatunation pulses and respiratory compensation were used. Irregularly thickened gallbladder wall is directly invading the adjacent liver panenchyma (open arrows), which is hypointense on
Ti-weighted is more
images apparent
nowheads, and
hyperintense
Ti-weighted
artery
that of the slightly on Ti-weighted definitely weighted pamenchyma.
(curved
on T2-wcightcd
images
a) in the hepatoduodenal
hepatic
vasion
(a) and
on
arrow,
in this
ligament a) are
also
primary tumor, that is, definitely hypointense on images and slightly or hypenintense on T2images relative to the liver In some cases liver in-
or metastasis
was
more
appan-
ent on T2-weighted images (Figs i, 2, 8), in others they were more apparent on Ti-weighted images (Figs 5, 9), and in still others they were demonstrated equally well on both sequences. There was no case of liver invasion or metastasis that was depicted only on one sequence. In nine cases, the primary tumor
Volume
174 #{149} Number
1
case.
that clearly
images
Nodular
involve
(b). Direct
and
the portal
demonstrated
liven
infiltrative on
vein
invasion
masses
(straight
Ti-weighted
(an-
arrow,
a)
images.
was separated from the duodenum by high-intensity fatty tissue on Tiweighted images. No duodcnal invasion was found at surgery in any of these cases (Fig lOa). In the remaining 10 cases, the fatty tissue plane between the primary tumor and the duodenum was obliterated in at least one section on Ti-weighted images. At surgery, however, duodenal invasion was confirmed in six of these 10 cases (Fig iob). In the other four cases, the primary tumor did not invade but merely abutted the duodenurn (Fig iOc). On T2-weighted images, it was difficult to identify the
the lesions were smaller than 1.5 cm. The tumor extension to these negions was definitely hypointense on Ti-weighted images relative to the surrounding fatty tissue or the pancreas and was slightly hyperintense on T2-weighted images. Thus, the contour of the tumor and its relationship to blood vessels and the pancreas were clearly demonstrated on Tiweighted images (Figs 2-6) but were usually unclear on T2-weighted images (Fig 5). In three cases, however, T2-weighted images helped differentiate nodal metastasis from the infenior tip of the caudate lobe of the liven (Fig 7). In these cases, nodal metastasis showed definitely higher signal intensity than did liven parenchyma on T2-weighted images, but the signal intensities were nearly identical on Ti-weighted images. In eight cases MR imaging also demonstrated a dilated bile duct associated with tumom extension to this region. The dilated bile duct was hypointense on Ti-weighted images and hyperintense on T2-weighted images when compared with the surrounding tissue and liver parenchyrna (Fig 3). When spatial presaturation pulses were used, the lumen of the portal vein exhibited no signal intensity whether it was encased by tumor or not. Without use of spatial presaturation pulses, high signal intensity due to slow flow in the portal vein was sometimes observed that mimicked portal vein thrombosis. However, these signals could be easily differentiated from those of tumor thrombus by the changes in their size and location on other sequences, by the presence of a uniform signal-free zone surrounding them, and by their prefenential occurrence on entry-side sections. CT findings were available in 15 cases. Non-contrast-enhanced studies were performed in three cases, contrast-enhanced studies were per-
Radiology
#{149} 133
7a.
6. Figures
6, 7.
Tumor
extension
to the
7b.
hepatoduodenal
ligament
and
paraaortic
region
on
(6) Ti-weighted
(600/20),
(7a)
Ti-weighted
(600/
25), and (7b) T2-weighted (2,000/60) MR images. Spatial presaturation pulses are used. (6) Severe infiltrative tumor is identified from the hepatoduodenal ligament to the paraaortic region. Arteries (curved arrows), portal vein (straight arrow), and pancreas are involved. Liver invasion is also present. (7) Liver invasion in the media! segment was minimal at surgery, but the tumor is almost isointense with the liver parenchyma on both sequences (arrowheads) and is difficult to identify. Lymph node metastasis confirmed at surgery is noted in the portocaval space (straight arrow). Differentiation of nodal metastases from caudate lobe of the liver (curved arrow) is difficult on Ti-weighted images (7a) but is easy on T2-wcighted images (7b) because the nodal metastasis is usually hyperintense relative to the liven parenchyma.
formed in four, were performed was direct liven liven metastasis
CT than
with
and both in eight. invasion depicted
MR imaging.
studies In no case or distant better with
In one
case, liver invasion and metastasis were not seen on CT scans but each was depicted on MR images. In all cases in which the primary tumor was close to the duodenum, the fatty tissue plane between them was obscured on CT scans regardless of the presence or absence of actual duodenal invasion. In cases of tumor extension to the hepatoduodenal ligament and paraaortic region, CT demonstrated round or nodular tumor spread as well as did MR imaging. However, when the tumor spread cxhibited infiltrative form, the contour of the tumor and the relationship of the tumor to surrounding structures were often unclear on CT scans (Fig 2).
8a.
9a.
Sb.
9b.
Figures
8, 9. (8) Multiple distant liven (600/25) and (b) T2-wcightcd
weighted rows) and distant (a) and hyperintense on
the
T2-weightcd
image.
(9) Multiple
liven
in this
often be successful
ability of the equipment. Additionally MR imaging does not seem to contribute to the detection of small tumors. Despite the prevalence of US screening, the majority of cases of gallbladder carcinoma still are not di-
easily resected (i-3). For the treatment of gallbladder carcinoma, therefore, it is important to detect this tumor in earlier states (16), that is, to detect small pmotmusions or irregular gallbladder wall thickening.
134 #{149} Radiology
In this
regard,
US
is the
direct
liver
metastases
on
invasion
on
(a) Ti-
Both direct liver invasion (anon the Ti-weighted image nodules are more apparent
(a) Ti-weighted
(600/20)
MR images. Spatial presatunation pulses and respiratory nodules (arrows) are more apparent on the Ti-weighted
The prognosis for patients with gallbladder carcinoma is extremely poor; however, this is mainly due to the prevalence of late diagnoses. Tumon confined to the gallbladder can
most
and
(2,000/60) MR images. liver metastasis (arrowheads) are hypointense on the T2-weighted image (b). Metastatic
(b) T2-weighted (2,000/60) sation were used. Mctastatic
DISCUSSION
metastases
and
compenimage
case.
useful
performance,
modality with low cost, and
its ease of the avail-
agnosed until the tumor has extended beyond the gallbladder (4). Liver invasion and extension of the tumor to the hepatoduodenal ligament frequently occur and have prevented tumor resection (i,2,i7,18). These tumom spreads require extended surgical approaches, such as lobectomy of the liven, lymph node resection with
January
1990
b. Figure
10.
Evaluation
for
duodenal
image. The tumor (arrowheads) and duodenum. (b) Case 2. Ti-weighted nal invasion was confirmed denum (*) but was found
invasion
c. in three
cases.
Arrow
the duodenum (*) are separated (600/25) MR image. The tumor
at surgery. (c) Case 3. Ti-weighted at surgery not to invade the duodenum.
netropancrcatic
nodal
(600/20)
MR
image.
The
tumor
skeletonization of the hepatoduodenal ligament, and even portal vein resection and pancreaticoduodenectorny. The standard surgical approach for advanced gallbladder carcinorna is not established and is still controversial (1-4,16-21). Diagnosis of gallbladder carcinoma may be facilitated by applying the established US and CT criteria to MR imaging (5,6,9-11). In massive-type tumors, the primary tumor mass by itself is often diagnostic of galibladden carcinoma. As has been previously reported (12-15), MR imaging can depict gallstones, including lucent stones trapped within the tumor. When a large mass of obscure origin occupies the subhepatic space, the presence of stones might be a clue to its primary organ (5,6,15). It is sometimes difficult to differentiate infiltrative-type tumor from inflammatory disease (6,9-il). This study did not evaluate the mole of MR imaging in the differentiation of infiltrative gallbladder carcinoma from chronic inflammatory disease. Both the appearance of the gallbladder (9) and the presence of tumor spread beyond the gallbladder, however, often enable the diagnosis of gallbladder carcinoma. The depiction of various modes of tumor spread will not only contribute to the staging of the gallbladder carcinoma but also aid in the differentiation of inflammatory from neoplastic disease. Direct liven invasion and distant liven metastasis were well displayed at MR imaging. The depiction of these lesions depends on the signal contrast between them and the nonmal liver, the size of the lesions, and
vasion was minimal, and MR imaging depicted all the lesions depicted at CT. MR imaging, therefore, performed at least as well as CT in the detection of liver invasion and metastasis. It has been shown (22) that optimal contrast for depicting liver metastasis is obtained with long TRs and TEs. In our series, however, results with Tiand T2-weighted MR imaging were inconsistent. We think, therefore, it is preferable to use both sequences for evaluating liver invasion and metastasis. Duodenal invasion was often overestimated when the criteria for invasion was the obliteration of the fat plane. Ti-weighted images can provide good signal contrast between fat tissue and the tumor and the duodenum. However, the fat plane between them can be readily obscured even in cases without invasion, pmobably secondary to respiratory motion artifacts, partial volume effects, and paucity of fat, as have been demonstrated with CT. Although techniques for reducing respiratory motion artifacts and varying the directions of the imaging plane may resolve these problems to some degnee, MR imaging has not yet sufficiently overcome these problems to accurately demonstrate duodenal invasion. Gallbladder carcinoma readily cxtends to the hepatoduodenal ligament and paraaortic region by means of various routes. In addition to lymph node metastasis, direct, vasculam, and penineural spreads have been reported as routes to this region (23). Moreover, lymphatic spread readily
the direction not detected ways small
goes beyond the limits of the phatic system (24). Infiltrative nodular tumors in this region
Volume
of the invasion. Lesions at MR imaging were alon the extent of tumor in-
174 #{149} Number
1
metastasis.
by a thin fat layer. At surgery, mass cannot be separated from
lyrnand are
(a) Case 1. Ti-weighted (600/20) MR the tumor was found not to invade the the duodenum (arrowhead), and duode-
(arrowheads)
is not
separated
from
the
duo-
considered a reflection of these types of spread. As previously reported (25,26), tumor contour and the nelationship of the tumor mass to the sunrounding structures, such as blood vessels and the pancreas, were often unclean at CT. This was encountered particularly when the tumor exhibited infiltrative form because of motion artifacts, poor contrast between the tumor and these structures, and inadequate contrast-enhancement techniques. US has also been reported to have limited potential for the evaluation of infiltrative tumor in this region (26). On the contrary, MR imaging depicted tumor spread in this region well and clearly demonstrated its contour on Ti-weighted images with high contrast between the tumor and the surrounding fat tissue. Moreover, the high contrast compared with the pancreas and the signal void of blood vessels were clearly revealed on this sequence, similar to the findings Doom et al meported for cholangiocarcinorna (i4). Although correlations with surgical results were limited for these findings, MR imaging appears effective in the evaluation of tumor spread to this region. Dilatation of the bile duct caused by tumor invasion also can be recognized, as has been meported (13,14). Because signal contrast between the tumor and surrounding fatty tissue is poor on T2-weighted images, tumor spread to this region is often better evaluated on Ti-weighted irnages. T2-weighted images will help in differentiating nodal metastasis from the caudate lobe of the liven. Only axial images were available in this series, but additional coronal or sagittal images would be helpful depending on the direction of tumor
Radiology
#{149} 135
invasion ed vessels. Because tive, and
and
the
course
of the
invad-
this study was retnospecthe correlation of MR findings to the surgical results was limited, only preliminary conclusions can be made concerning the ability of
MR imaging to demonstrate the vanous modes of spread of gallbladder carcinoma. Furthermore, it remains to be determined if MR imaging can depict small, differentiate tory lesions. found
the
that
extent
early-stage them from In conclusion MR
tumors and inflamrnawe have
imaging
can
of gallbladder
and can contribute this disease. U
depict
staging
1.
2.
8.
9.
MA.
Carcinoma
1216. Morrow
of the gallbladAm 1973; 53:1203DER,
Florack
vant 714. Muir
Itai Y, Anaki
chemotherapy. IM, Morris
gallbladder.
Surgery DL.
Br J Hosp
1983;
Carcinoma
Med
14.
is. i6.
1986; 36:278-
imaging
17.
Dooms
U!cur-
21.
GC, Kerlan
23.
on autopsied
cases. Tan to Sui
i983;
24.
4:i2.27-i24i. [Japanese] Klamer TW, Max MH. Carcinoma gallbladder. Sung Gynecol Obstet
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156:641-645. CB, et a!.
biliary
25.
RK Jr. Hricak
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Higgins
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Fhairn RB, Ferris DO, McDonald JR. et a!. Carcinoma of the gallbladder: an appraisal of its surgical treatment. Arch Sung i963; 86:176-183. Hamnick RE Jr. Liner FJ, Hastings PR, et a!. Primary carcinoma of the gallbladder. Ann Sung 1982; i95:270-273. Sakaguchi 5, Nakamura S. Surgery of the portal vein in resection of cancer of the hepatic hilus. Surgery 1986; 99:344-349. Takasaki K, Kobayashi S. Mutoh H, et a!. Our experience (5 cases) of extended right lobectomy combined with pancreaticoduodenectomy for the carcinoma of the gallbladder. Tan to Sui 1980; 7:923-932.
Uapanese] 22.
Corn-
Ra-
Rossmann MD, Friedman AC, Radecki PD, et a!. MR imaging of gallbladder carcino-
26.
M, Clark
and imaging
LR, et al.
spectrum
of pan-
creaticoduodenal lymph node enlargement. AJR 1985; i44:i223-i227. Baker ME, Silverman PM, Halvorson Jr. et a!. Computed tomography of masses in peritoncal/hepatoduodena!
ament.
J Comput
Assist
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11:258-263.
Primary
carci-
Sung Clin North
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20.
carcino-
of the gallbladder.
ogy 1983; 147:481-484. Dooms GC, Fisher MR.
noma
280.
i36
K, et a!.
Cholangiocarcinoma: imaging diology 1986; i59:89-94.
94:709-
of
Thorsen MK, Quiroz F, Lawson TL, ct a!. Primary biliary carcinoma: CT evaluation. Radiology 1984; 152:479-483. Hricak H, Filly RA, Margulis AR, et a!. Work in progress: nuclear magnetic reso-
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Piehlem JM, Crichlow RW. Primary carcinoma of the gallbladder. Surg Gynecol Obstet 1978; 147:929-942. Adoson
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