Interventional Showkat Ghulam
A. Zargar, MD, DM M. Jan, MD #{149} Parveen
US-guided of Gallbladder
#{149} Mohammad
Shah,
approach.
Pain,
a minor
complication of the procedure, was noted in four cases. No instances of hemorrhage or vasovagal reactions occurred. From their experience in this large series, the authors condude that US-guided fine-needle aspiration biopsy of gallbladder masses is a safe, reliable, and accurate technique for the diagnosis of malignancy.
MD,
DM
#{149} Rakesh
Aspiration
ECENT
reports
have
ma without surgery. The size of masses in the gallbladder ranged from 2.0 X 1.8 to 4.8 X 3.3 cm in diameter.
established
the safety, reliability, and costeffectiveness of ultrasound (US)guided fine-needle aspiration biopsy in the diagnosis of lesions of the er, pancreas, kidney, and lymph nodes (1). However, interventional
liv-
radiologists
to
have
been
perform percutaneous the gallbladder for
ly causing
bile
however, the safety
reluctant
A sterile
puncture of fear of accidental-
peritonitis.
reports have of US-guided
Recently,
tized
demonstrated puncture
of
the gallbladder for a variety of diagnostic and therapeutic purposes (28). Application of US-guided aspiration biopsy for the evaluation of gallbladder
masses
series
has been limited to cases (3,8). We report with this procedure who demonstrated
of small
our experience in 88 patients
gallbladder masses smaller cm in diameter. US-guided
dle aspiration a safe, enabling
biopsy
reliable, the
was
found
der, neoplasms, thickening,
762.321
#{149} Gallbladder,
wall
762.929
Radiology
1991;
MATERIALS
AND
to be of
METHODS
Over
the last 3 years, 648 patients with biliary diseases were evaluated by us. The majority of these patients were referred
from
other
tion is the only cal center in the gent population million people. patients
who
hospitals.
Our
institu-
specialty-oriented mediarea and serves an mdiof slightly more than 4.2 Eighty-eight consecutive
were
suspected
of having
carcinoma of the gallbladder on the basis of clinical and US data were included in our study. The group comprised 38 men and 50 women, who ranged in age from 49 to 71 years,
I
From
the
Departments
of Gastroenterology
(S.A.Z., M.S.K., R.M.) and Cytology (G.M.J., P.S.), Institute of Medical Sciences, P0 Box 27, Srinagar (Kashmir), India 190 011. Received June 7, 1990; revision requested July 13; revision received November 8; accepted November 19. Address reprint requests to M.S.K. c RSNA, 1991
with
a mean
age
of 53
years. The most frequent complaints of the patients were right upper quadrant pain and jaundice due to obstruction of the bile duct, which were present in 62 patients. Among other complaints were painless palpable masses in the right hypochondrium in 17 patients and ascites in five. The main indication for performing fine-needle aspiration biopsy was to confirm
the
presence
of gallbladder
carcino-
(Aloka
by injection
of 2% lidocaine
(Xylo-
caine; Astra, Westboro, Mass). The distance from the center of the lesion to the skin was measured by means of electronic calipers. The needle, enclosed in a stylet, was nel,
inserted during
was then attached
various 179:275-278
transducer
through suspended
the guiding respiration,
chanto the
point that the tip of the needle reached the center of the mass (Fig 1). The stylet
than 4.8 fine-nee-
and accurate means diagnosis of gallbladder
puncture
SSD 256; Aloka, Tokyo), with a preset puncture area and guiding channel, was used to locate the mass. A 22- or 23-gauge, beveled, Teflon-coated needle (Cook, Bloomington, Ind), which can be seen easily on sonograms, was used for aspiration biopsy. Following skin cleansing, the selected skin entrance site was anesthe-
#{149} Bi-
in-
MD
Biopsy
masses. Index terms: Bile ducts, biopsy, 762.1298 opsies, technology, 762.1298 #{149} Gallbladder, terventional procedure, 762.12985 #{149} Gallblad-
Mahajan,
MD
Fine-Needle Masses’
Ultrasonically (US) guided fine-necdie aspiration biopsy was performed in 88 patients who had gallbladder masses. All masses were less than 4.8 cm in diameter. A 22- or 23gauge, Teflon-coated needle was placed into the mass with the transhepatic or transperitoneal route. By means of this technique, gallbladder malignancy was confirmed in 69 of the 78 cases of malignancy (88.5%). Ten of 10 benign lesions were properly categorized. One patient developed bile peritonitis following a single needle pass with the transperitoneal
S. Khuroo,
Radiology
removed. to the hub
A 20-mL syringe was of the needle, and as-
piration biopsy was performed by backand-forth movements of the needle under continuous negative pressure, which was created by the application of adequate gentle suction with the syringe. The suction was then gently released and the needle withdrawn out of the lesion. The aspirate was deposited onto one to three clear glass slides, smeared, air-dried, and stained with May-Gr#{252}nwald-Giemsa stain. Additional special stains were used as necessary.
The
aspirates
were
submit-
ted for microbial culture tests if an infectious process was suspected. The aspiration procedure was repeated if, on visual inspection, the amount of material obtamed was inadequate. However, no more than three aspirations were done at any one time. Antibiotics were usually administered before the procedure if an infectious process was suspected. After the procedure, patients were observed in the standard manner. All patients were in-patients at our institution. In the first 43 patients, aspiration was performed either via the transhepatic route or directly through the anterior wall
of the
gallbladder,
without
passing
through the liver parenchyma (the anterior transperitoneal route); however, in the last 45 patients, only the transhepatic approach was used. Cytologic specimens were classified as negative or positive for malignancy on 275
the
basis
cal
purposes,
of standard
criteria.
patients
diagnosed
as “positive”
amination
were
those
whose
or
were
at cytologic
ex-
fh..
positive;
were
diagnosed
“suspicious
“unsatisfactory”
---
statisti-
lesions
considered
lesions
“negative,”
For
whose
as
for malignancy,”
were
considered
to be
negative. All analyses
were
significantly less
performed
x2 test. Results
of the
different
than
or equal
with
use
considered if the P value
was
were
to .05.
-
RESULTS A total
of
a.
1 18 US-guided
Figure
fine-nee-
dle aspiration biopsies were completed in 88 patients. The biopsies, by means of one to three needle passes, were performed in one sitting for 83 patients and in two sittings for five. Seventy-eight patients (88.6%) were diagnosed as having gallbladder malignancies. The final diagnosis of malignancy was made on the basis of findings at subsequent histologic examinations of surgical specimens, lymph
nodes,
and
metastases
b.
genic
owing
of malignant
needle lymph ascitic tients
cells
c.
sonogram the whole
(small
(arrowhead). stain;
demonstrating gallbladder
arrow).
gallbladder arrow).
(large
(b) Teflon-coated
(c) Fine-needle original magnification,
carcinoma Gallstones
needle
aspirate shows X100).
is seen
Diameter
shows an echowith acoustic shad-
within
adenocarcinoma
Table 1 Results of Fine-Needle Aspiration Biopsy of Gallbladder Comparing Tumor Size and Appearance at US
the mass cells
during
(May-Gr#{252}n-
Malignancies,
of Lesions
(cm) Total
in 59 of
Appearance Mass
partly
filling
at US or totally
polypoid
No.
2.5
2.6-3.5
3.6-4.8
of Cases
5 (4)
29 (26)
27 (24)
61 (54)
3 (3)
5 (4)
5 (5)
13 (12)
3(2)
1(1)
11 (9)
35 (31)
the gallbladder
Intraluminal masses
Thickeningofthe wall of the gallbladder Totals
in fine-
aspirates obtained from nodes, metastatic deposits, or fluid. Sixty-four of the 78 pa(82.1%) had associated gall-
(a) Transverse that occupies
are also seen
aspiration wald-Giemsa
the 78 cases (75.6%). In the remaining 19 patients, malignancies were reasonably confirmed on the basis of available clinical data and demonstration
1. mass
Note-Numbers in parentheses with use of fine-needle aspiration
indicate biopsy.
number
4(3)
...
32 (29)
of patients
whose
tumors
78 (69)
were
correctly
diagnosed
stones.
Three patterns of primary carcinoma of the gallbladder were recognized (Table 1). The most common pattern, found in 61 cases, was an echogenic inhomogeneous mass that
polypoid masses was well (Fig 3). The 13 intraluminal were located in the fundus
partly
gallbladder
or totally
ic lumen of sharp bladder
occupied
the
of the gallbladder, definition between and liver parenchyma
1, 2). In these
61 cases,
the
anecho-
with loss the gall(Figs gailblad-
der was totally replaced by a mass in 42 cases, and a mass obliterated more than four-fifths of the lumen in the other 19 cases. The masses were situated along the anterior wall of the gallbladder in 1 1 cases and along the posterior wall in eight. Another pattern was thickening of the gallbladder wall, occurring in four cases; the margins of two of these masses were irregular, with inhomogeneous echo patterns. Wall thickness was diffuse in one
case
was
found
cases
and
and
along along
focal
the the
in three
fundus anterior
and
in wall
two
in
one. Wall thickness ranged from 1.2 to 2.7 cm (mean, 2.0 cm). The third pattern, intraluminal polypoid masses, was found in 13 cases that showed echogenic masses within the gallbladder lumen; the shape of these 276
Radiology
#{149}
in six
cases,
recognized masses of the the
neck
value of a positive result There were 10 patients proved benign diseases, in
two, the anterior wall in three, and the posterior wall in two. Among the 78 patients with malignant tumors, fine-needle aspiration biopsy
enabled
correct
diagnosis
in
69 patients, resulting in a sensitivity of 88.5% (Table 2). The results at cytologic examination were suspicious for malignancy in three cases, negative in four, and unsatisfactory in two. The suspicious diagnoses were issued for those cases in which cytologic findings were suggestive but not absolutely diagnostic for a malignant
neoplasm.
Patients
from
whom
no cellular material could be obtamed were considered to have “unsatisfactory” samples. In the four cases diagnosed as “negative,” inflammatory cells, necrotic material, and/or columnar cells were obtained in the aspirate. The sensitivity for the first 40 malignant masses was 80%, and it increased to 97.4% for the subsequent 38 masses. The predictive
had
inflammatory
bladder,
was 100%. with all of whom
lesions
of the
as well as gallstones. had acute cholecystitis.
patients
gall-
Eight The
other two had painless, palpable masses in the right hypochondrium; chronic cholecystitis with superimposed empyema was found at surgery. Aspiration biopsy was undertaken because of the presence of one or more of the following features at US: thickened (6-14 mm) gallbladder
wall,
found
ly thickened in
four;
gallbaldder nondependent
material men, genic
in six patients;
within found material
the
in two; that
when
the
patient
found
in three;
between
and
fine-needle lesions
shift
position,
irregularly
marginat-
collections,
the
of sharp
gallbladder
patic parenchyma, All 10 patients all
luecho-
changed
lack
aspiration
found
definition
wall
found underwent
correctly
found
gallbladder dependent did not
ed pericholecystic in two;
irregularwall, echogenic
and
he-
in three. successful
biopsy,
with
categorized
as April
1991
algesics (1.1%) and
for 48 hours. One patient developed biliary peritonitis
required
surgery;
afterward,
the
patient recovered completely. This 65-year-old man had a lesion that was 3.6 X 2.5 cm in diameter, and the aspiration procedure yielded adequate material with a single needle pass via the transperitoneal route.
bilia,
None
tonitis. Theoretically, may plug any potential
liver
for
of a larger
of the
patients
hemorrhage
experienced
or vasovagal
reactions.
DISCUSSION ‘:
c :
#{241}
.
3.
Figures
2, 3.
(2) Longitudinal
anterior
scan
demonstrating gallbladder carcinoma shows an echogenic mass within the gallbladder that is causing obstruction at the common hepatic duct, with dilatation of hepatic ducts. GB = gallbladder, CHD common hepatic duct. (3) Transverse scan through right hypochondrium demonstrates gallbladder carcinoma and shows an intraluminal polypoid mass within the gallbladder. Ascites is also seen. GB gallbladder.
Table 2 Cytologic Results of US-guided FineNeedle Aspiration Biopsy of the Gallbladder versus Final Diagnoses at Pathologic Examination Final
Diagnosis
Malignant Cytology
Results
(it
Positive Suspicious Negative Unsatisfactory
=
Benign (n 10)
78)
69 (88.5%) 3 4 2
The present large series shows that US-guided fine-needle aspiration biopsy of gallbladder masses is a safe, reliable, and highly accurate method of enabling correct diagnosis of malignancies. The overall accuracy of cytologic evaluation of aspirates was 89.8%, with a sensitivity of 88.5% and a specificity of 100%. The predictive values sults
ficity
thus
of 100%.
tive value tory nature recognized trophils
The
yielding
sis of the
was 52.6%. The of the lesions by the presence and
necrotic
predic-
results
that
for
malignancy.
Eight
due
in part
gained
by both
diologist
and
to the
the the
experience
interventional cytologist.
raUnsuc-
cessful,
and
surgical
biopsy
should
be
of tumor cells in the aspirate. of the aspirates grew Escherichia coli bacteria in three cases and Kiebsiella aerogenes bacteria in one. The choice of antibiotics was changed in one case on the basis of the results of these cultures. The overall accuracy of fine-needle aspiration biopsy to enable correct diagnosis of all gallbladder lesions was 89.8% (79 of 88 cases). The diag-
performed. Provided that aspirates are adequate for cytologic analysis, a positive result (ie, the smear shows unequivocally malignant cells) should
nostic
in our tients
the lack Cultures
yield
the
had
no
relationship
to
size (P > 1) or appearance at US (P > .1) of gallbladder malignancies (Table 1). Four patients (4.5%) developed minor
.
complications,
of mild abdominal pain that required
Volume
179
#{149} Number
which
consisted
or right the use
shoulder of mild
I
strongly
support
malignant tive test caution,
lesion. However, a negashould be interpreted with especially when clinical sus-
picion nearly
diagnosis
for malignancy one-half of the series with
is high, negative
of a
since tests
were obtained in pamalignant disease.
In this series, no procedure-related deaths occurred, but biliary peritonitis developed in one patient whose biopsy was obtained the transperitoneal
an-
the
of the
transperitoneal
by puncture via route. Proponents
approach
ar-
can
be
avoided
if there
is no
need for a needle to pass through the liver (3). However, there are also problems with the transperitoneal route, including the potential for bile leak, puncture of the colon, and pentissue
gallbladder leak, thus lessening the likelihood that leaking of free intrapenitoneal bile will occur. Plugging the transhepatic needle track with absorbable gelatin sponge (Stenispon; Allen & Hanburys, Middlesex, England) may reduce the frequency of serious cornplications (9); however, this procedune may not be necessary if a thin needle is used for hepatic puncture. Such a technique may be appropriate repair
of the
track
cath-
eter or following core biopsy. Likewise, the risk of major hemorrhage would be reduced with use of the transhepatic route, since the peniphery of the liver would be avoided, as well as the large vessels in the porta hepatis and peniportal regions. Moreover, assessment of the anatomic relationship of the gallbladder to the liver and right hemicolon showed that, in most patients (83%), percutaneous
of
cessful aspiration of a focal lesion should prompt a repeat procedure, and, if the repeat procedure is unsuc-
inflammawas easily of neu-
material
false-negative
were obtained in nine cases revealed that samples either lacked cellular material, contained cellular material that was suggestive of a benign process, or contained material that was the nine false-negative results were obtained from the first 40 cases, as well as in one additional case during biopsy of the subsequent 38 malignant masses. This marked improvement in results over the years
a speci-
negative
and negative reand 52.6%, respec-
tively. False-negative results are one of the main drawbacks to the use of fine-needle aspiration biopsy. Analy-
was
nonmalignant,
of positive were 100%
suspicious
0 0 10(100.09) 0
gue that the risk of accidental hepatic injury, which can be accompanied by intraperitoneal hemorrhage or hemo-
access
via
the
shortest
distance
would require transhepatic puncture (10). While no controlled study has been conducted to evaluate the validity of these points, we concur with others (3,8) that the transhepatic approach is preferred. Other complications reported with gallbladder puncture include severe vasovagal reactions, hypotension, peritonitis, bacteremia, and hemobiha (2-8). Gallbladder cancers do not lend themselves to early diagnosis; the majority of these malignancies are stage III or IV when first diagnosed (1 1
Moreover,
).
sonographic
differ-
entiation of a benign, inflammatory lesion from a cancerous mass is not reliable. Therefore, histologic diagnosis becomes mandatory from a prognostic and therapeutic standpoint. Two cases of early gallbladder cancer were diagnosed in this study. We
believe
real-time piration
that
the
US-guided biopsy
extensive
use
fine-needle
of small
solid
of
asgall-
bladder masses will contribute to the early diagnosis of gallbladder cancers and obviate the need for diagnostic laparotorny in patients with advanced
malignancies
are poor surgical needle aspiration
or those
who
risks. Hence, finebiopsy of gallbladRadiology
#{149} 277
den masses the
can
treatment
beneficially of many
Acknowledgment: PA, for secretarial
influence patients.
We thank
U
4.
ous gallbladder procedures. 1986; 160:23-26. Illescas FF, Braun SD, Cohan
JD, Dunnick
Mehraj-ud-Din,
biliary
References 1.
M, Altmannsberg M, KehI A, et al. Ultrasound guided percutaneous fineneedle aspiration biopsy of abdominal
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and retroperitoneal 1984;
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vanSonnenberg al. Diagnostic
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nondilated
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Pearse S.
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E, Wittch CR, Casola C, et and therapeutic percutane-
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vanSonnenberg
E, Hofmann
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emus
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Neoptol-
RA, Wilwith
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JP, Lindfors
KK.
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cystitis: diagnostic accuracy of percutaneous aspiration of the gallbladder. Radiology 1988; 167:669-671. Teplick 5K. Diagnostic and therapeutic interventional gallbladder procedures. AiR 1989; 152:913-916. Tobin MV, Gilmore IT. Plugged liver biopsy in patients with impaired coagulation. Dig Dis Sci 1989; 34:13-15. Warren LP, Kadir 5, Dunnick NR. Percutaneous cholecystostomy: anatomic considerations. Radiology 1988; 168:615-616.
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MA, Farnell
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AJR
April
1991