AJR 2001; 176:797-802
© American Roentgen Ray Society
Multiple Bile Duct Biopsies Using a Sheath with a Side Port
Usefulness of Intraductal Sonography
Kiichi Tamada1,
Yukihiro Satoh,
Takeshi Tomiyama,
Akira Ohashi,
Shinichi Wada,
Kenichi Ido and
Kentaro Sugano
1
All authors: Department of Gastroenterology, Jichi Medical School, Yakushiji,
Tochigi 329-0498, Japan.
Received July 17, 2000;
accepted after revision September 12, 2000.
Address correspondence to K. Tamada.
Abstract
OBJECTIVE. We clarified the number of biopsies required to determine
malignancy of the biliary tract on the basis of the type of bile duct
tumor.
SUBJECTS AND METHODS. Patients with a biliary tract malignancy
(n = 33) and a benign biliary stenosis (n = 3) underwent
biopsy via the percutaneous transhepatic route. We performed intraductal
sonography using a 20-MHz probe with a 2.0-mm diameter. The sonographic
findings were prospectively classified as polypoid, circular, or semicircular.
The tip of a long 9-French sheath with a side port was wedged into the
stenosis, and six specimens were obtained with a 1.8-mm-diameter forceps with
serrated cups.
RESULTS. When cholangiography or intraductal sonography showed a
polypoid lesion, the sensitivity of two biopsies was 100% (6/6). When
cholangiography showed a stenotic lesion, the sensitivity of nine biopsies
(96%, 26/27) was superior to that of two biopsies (74%, 20/27; p <
0.05). When intraductal sonography showed a circular lesion, the sensitivity
of three biopsies (100%, 14/14) was superior to that of a single biopsy (64%,
9/14; p < 0.05). When it showed a semicircular lesion, the
sensitivity of nine biopsies (92%, 12/13) was superior to that of two biopsies
(54%, 7/13; p < 0.05).
CONCLUSION. Bile duct biopsy using a sheath with a side port has a
high sensitivity. However, the number of biopsies required depends on the
cholangioscopic and intraductal sonographic appearance of the tumor.
Introduction
Tissue sampling is essential for the treatment planning for biliary
strictures
[1,2,3,4,5,6,7,8].
Although percutaneous transhepatic biliary biopsy is a useful modality
[1,2,3],
to our knowledge, no report has delineated how many specimens should be taken
to confirm or exclude the diagnosis of malignancy of the biliary tract.
Additionally, because a variety of different tumors and types of tumors
develop in the pancreaticobiliary tree, biopsy guidelines may differ according
to the clinical presentation
[5]. In our study, intraductal
sonography was used to classify the type of tumor. Intraductal sonography with
a high-frequency thin-caliber sonographic probe produces high-quality
cross-sectional images of the bile duct. Intraductal sonography has been
reported to be useful for locoregional staging of biliary tract carcinoma
[9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27],
characterization of biliary strictures
[9,
10,
20,21,22,
26], assessing the effects of
radiation therapy [28], and
monitoring during microwave coagulation therapy with percutaneous transhepatic
cholangioscopy for bile duct cancer
[29]. To our knowledge, ours
is the first prospective study designed to define guidelines for percutaneous
transhepatic forceps biopsy with fluoroscopic control for the diagnosis of
biliary tract cancer.
Subjects and Methods
Subjects
Between October 1997 and May 2000, 33 patients with a biliary tract
malignancy and three patients with a benign biliary stenosis underwent
percutaneous transhepatic forceps biopsy after intraductal sonography and were
included in the study. The 24 men and 12 women had an average age of 68.7
years (age range, 41-84 years). All malignant lesions were confirmed by
transhepatic biopsy (n = 32) or surgical resection (n = 1).
All patients with benign lesions underwent percutaneous transhepatic
cholangioscopy and were observed clinically for more than 2 years.
Methods
Written informed consent was obtained from all patients before percutaneous
transhepatic biliary drainage, intraductal sonography, and biopsy. All
procedures were conducted with IV anesthesia (10-mg diazepam and 15-mg
pentazocine). Broad-spectrum antibiotics were administered prophylactically
for drainage and biopsy procedures. A few days after percutaneous transhepatic
biliary drainage, the bile duct was cannulated with a presharpened catheter
(PD-JA6.5F; Catex, Tokyo, Japan) and a polymer-coated guidewire (Radifocus;
Terumo, Tokyo, Japan). After exchanging the guidewire for an extrastiff
guidewire (Amplatz; Cook, Bloomington, IN), we introduced a 9-French
250-mm-long sheath with a side port (RS-A90K25A, Terumo) into the bile duct
over the guidewire. Then, a 2.0-mm-diameter sonographic probe with a frequency
of 20 MHz (MP-PN20-06L; Aloka, Tokyo, Japan) was inserted into the bile duct
along the guidewire through the sheath with fluoroscopic guidance. The tip of
the probe had a side slit for the guidewire. The catheter generated
high-resolution real-time cross-sectional images with an axial resolution of
0.1 mm and a maximum penetration of approximately 20 mm. Contrast medium (30%
meglumine sodium amidotrigoate) was injected through the side port of the
sheath. The gross appearance of the mass and the tumor extension to the
hepatic artery, portal vein, pancreatic parenchyma, and adjacent structures
were estimated on sonograms according to previously reported criteria
[12,13,14,15,16,17].
After reviewing the images, we withdrew the ultrasonic probe. Then, biopsies
were performed with forceps with serrated cups without a needle (FB-52C-1;
Olympus Optical, Tokyo, Japan). The 1.8-mm-diameter forceps could be rotated.
The tip of the sheath was wedged inside the stenosis. The forceps were
inserted through the sheath and introduced into the stenosis with fluoroscopic
guidance (Fig. 1). The location
of the sheath and forceps was confirmed by the injection of contrast medium
through the side port of the sheath. More than six specimens were obtained.
The tip of the forceps was rotated for each specimen. When cholangiography
showed a stenotic lesion, specimens were obtained at several depths including
the inside and margins of the stenosis. Polypoid lesions also were biopsied at
several depths. The biopsy specimens were fixed in 10% formalin, stained with
H and E, and analyzed by two experienced pathologists. After completing the
biopsies, we removed the sheath, and an internal-external drainage catheter
was inserted over the guidewire.
Study Design
When histologic examination of the six initial specimens showed no
malignancy, six additional biopsy specimens were obtained with fluoroscopic
control, and six other biopsies were obtained with percutaneous transhepatic
cholangioscopy. The additional specimens were taken with fluoroscopic guidance
with the sheath as described previously. In performing cholangioscopy, we
dilated the percutaneous tract to 16-French with the coaxial catheter
[30], and biopsies were
performed with direct vision by cholangioscopy. Three biopsy specimens were
taken from the margin of the stenosis, where the dilated vessel was used as a
landmark for tissue sampling, whereas the other three specimens were obtained
from within the area of stenosis
[5]. When intraductal
sonographic findings were highly suggestive of cancer
[21], surgical resection was
performed even if none of the biopsies revealed a malignancy. The
cholangiographic findings were classified as polypoid or stenotic
[31] by two experienced
reviewers before intraductal sonography and biopsy. The intraductal
sonographic findings were classified as polypoid, circular, or semicircular
(Figs.
2A,2B,2C,3A,3B,3C,3D,4A,4B,4C,5A,5B,5C).
When the width of the hypoechoic layer was thicker than that of the proximal
side in a circular fashion, it was classified as circular (Figs.
2B and
4A,4B,4C).
The sonograms were prospectively reviewed by two experts, including the first
author, without knowledge of the findings on other imaging examinations except
those of extracorporeal sonography and cholangiography. The data were analyzed
with Fischer's exact test. A p value less than 0.05 was considered
significant.
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Fig. 2A. —Drawings show schema of sonographic findings. Arrow at bottom
of drawings shows scanning from proximal side to center of tumor. Drawing of
sonogram shows polypoid lesion with narrow base. T = tumor, BD = bile duct,
left = proximal side of tumor, right = center of tumor.
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Fig. 2B. —Drawings show schema of sonographic findings. Arrow at bottom
of drawings shows scanning from proximal side to center of tumor. Drawing of
sonogram shows circular lesion and circumferential thickening of bile duct by
tumor (right). At center of tumor (T), width of lesion (distance between probe
and outer margin of tumor, B) is thicker than width of bile duct (BD) wall
(inner hypoechoic layer, A) of proximal side. left = proximal side of tumor,
right = center of tumor.
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Fig. 2C. —Drawings show schema of sonographic findings. Arrow at bottom
of drawings shows scanning from proximal side to center of tumor. Drawing of
sonogram shows semicircular lesion and eccentric thickening of bile duct by
tumor (right). At center of tumor (T), width of hypoechoic layer of thinnest
side (B) is equal to that of proximal side (A). BD = bile duct, left =
proximal side of tumor, right = center of tumor.
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Fig. 3B. —84-year-old man with common bile duct cancer (polypoid lesion
on sonograms). Sonogram shows polypoid lesion (arrowheads) with
narrow base (arrow) at proximal side of main tumor (T). BD = bile
duct.
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Fig. 3D. —84-year-old man with common bile duct cancer (polypoid lesion
on sonograms). Histologic examination of resected specimen shows cancer cells
in entire polypoid tumor (arrowheads). (H and E, x2)
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Fig. 4A. —68-year-old man with common hepatic duct cancer (circular
lesion on sonograms). Sonogram shows wall thickening (arrowheads) at
proximal side of main tumor (T). Arrows = width of bile duct, BD = bile duct,
A = inner hypoechoic layer.
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Fig. 4B. —68-year-old man with common hepatic duct cancer (circular
lesion on sonograms). Sonogram at center of tumor (T) shows tumor around probe
in circular fashion (arrowheads). In this position, distinction
between polypoid lesion (Fig.
3C) and circular lesion
(Fig. 4B) is difficult.
At center of tumor, width of tumor (distance between probe and outer margin of
tumor, width of B) is thicker than width of bile duct wall (inner hypoechoic
layer, width of A in Fig.
4A) of proximal side.
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Fig. 4C. —68-year-old man with common hepatic duct cancer (circular
lesion on sonograms). Histologic examination of resected specimen shows cancer
cells in circular fashion in bile duct mucosa and submucosal tissue
(arrowheads). (H and E, x2)
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Fig. 5A. —66-year-old man with common hepatic duct cancer (semicircular
lesion on sonograms). Sonogram shows semicircular wall thickening
(arrowheads) at proximal side of main tumor (T). Arrows = width of
bile duct, BD = bile duct, A = proximal side of tumor.
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Fig. 5B. —66-year-old man with common hepatic duct cancer (semicircular
lesion on sonograms). Sonogram at center of tumor (T) shows tumor in
semicircular fashion (arrowheads). At center of tumor, width of
hypoechoic layer of thinnest side (width of B) is equal to that of proximal
side (width of A in Fig.
5A).
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Fig. 5C. —66-year-old man with common hepatic duct cancer (semicircular
lesion on sonograms). Histologic examination of resected specimen shows cancer
cells in semicircular fashion in bile duct mucosa and submucosal tissue
(arrowheads). (H and E, x2)
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Results
Clinical Course of Patients with Malignant Disease
Histologic examination of the first six specimens of each patient showed
adenocarcinoma in 31 of 33 patients. In one of the remaining patients,
histologic examination of the ninth specimen showed adenocarcinoma. In the
other remaining patient, none of the 18 specimens showed cancer. However,
examination of the surgically resected specimen showed adenocarcinoma.
Three patients were determined to have pancreatic cancer by surgical
resection (n = 1) or endoscopic retrograde pancreatography
(n = 2, stenosis of the pancreatic duct), although sonography showed
neither a pancreatic mass nor pancreatic duct dilatation. In four patients,
dynamic CT showed a gallbladder mass that was presumed to be gallbladder
cancer. The other 26 patients were determined to have bile duct carcinoma.
Surgical resection was performed in 11 of 33 patients. Another 18 patients
underwent percutaneous placement of a metallic biliary stent
[28]. The remaining four
patients underwent microwave coagulation of the tumor with percutaneous
transhepatic cholangioscopy
[29].
Clinical Course of Patients with Benign Disease
Histologic examination of 18 specimens did not show malignant cells in any
patient. Patients were diagnosed with primary sclerosing cholangitis
(n = 1), chronic pancreatitis (n = 1), or biliary stenosis
caused by a motor vehicle collision (n = 1). These patients were
treated by temporary placement of a biliary endoprosthesis. None of them
showed any sign of cancer on sonography, CT, or clinical reassessments for
more than 2 years.
Complications
Two patients suffered dislodgement of the biliary drainage catheter, and
they were successfully treated by a second drainage procedure. Although one
patient suffered transient biliary bleeding after biliary drainage, it
resolved without the need for transfusion or transarterial embolization. None
of the patients experienced cholangitis, bacteremia, perforation of the sinus
tract, or biliary bleeding as a result of biopsies.
Sensitivity Classified by Cholangiographic Findings
The pathologists found the amount of tissue to be sufficient in the initial
biopsy specimens in 31 of 33 patients and in the first two specimens in all
patients. When cholangiography showed a polypoid lesion, the sensitivity of
two biopsies was 100% (6/6) (Table
1). When cholangiography showed a stenotic lesion, the sensitivity
of two biopsies (74%, 20/27) was superior to that of a single biopsy (44%,
12/27). The sensitivity of nine biopsies (96%, 26/27) was superior to that of
two biopsies (p < 0.05).
Sensitivity Classified by Sonographic Findings
When intraductal sonography showed a circular lesion, the sensitivity of
three biopsies (100%, 14/14) was superior to that of a single biopsy (64%,
9/14; p < 0.05) (Table
2). When it showed a semicircular lesion, the sensitivity of five
biopsies (77%, 10/13) was superior to that of a single biopsy (38%, 5/13), and
the sensitivity of nine biopsies (92%%, 12/13) was superior to that of two
biopsies (54%, 7/13; p < 0.05).
Histologic Analysis of Resected Specimens
In the 11 patients with malignancy who underwent surgical resection (10
with bile duct cancer and one with pancreatic cancer), preoperative
intraductal sonography accurately assessed tumor invasion to the hepatic
artery in 10 patients and to the portal vein in 10 patients. It showed
polypoid (n = 1), circular (n = 5), and semicircular
(n = 5) lesions. In one patient with a polypoid lesion, histologic
examination of the resected specimen showed well-differentiated cancer cells
in the entire polypoid tumor. In five patients with circular lesions,
histologic examination of the resected specimen showed cancer cells arranged
in a circular pattern in the bile duct mucosa and submucosal tissue. In the
remaining five patients with semicircular lesions, histologic examination of
the resected specimen showed cancer cells arranged in a circular pattern in
only one patient, in a semicircular pattern in three patients, and in no area
of the bile duct mucosa in the remaining patient.
Discussion
Tsai et al. [1] have
performed percutaneous transluminal forceps biopsies, using a long sheath and
1.8-mm-diameter forceps. Although these researchers obtained three to five
specimens in each patient, the sensitivity was only 71%. They reported that
the main reason for failure was that the specimens were obtained only proximal
to the stenosis. Savader et al.
[2] have performed clam-shell
forceps biopsies with fluoroscopic guidance, using a sheath, with a
sensitivity of 75% in pancreatic carcinoma and 0% in cholangiocarcinoma. In
their study, the sheath was advanced to the level of the lesion, but not
across it. These researchers did not routinely perform multiple biopsies.
The sensitivity in our study is superior to sensitivities reported in these
conventional studies. Several factors may explain these results. First, the
biopsies were performed with 1.8-mm-diameter forceps with serrated cups that
could be rotated. Thus, sufficient material was obtained from all patients
with two biopsies. Second, the stenotic bile duct was successfully cannulated
in all patients, and the tip of the long sheath was advanced to the stenotic
area along the extrastiff guidewire. Third, multiple biopsies were routinely
performed at various depths in the stenosis. Furthermore, the sheath had a
side port for the injection of contrast medium after introduction of the
forceps. We obtained cholangiographic information about the stenotic lesions
during the procedure. This information was used to direct the biopsy forceps
to multiple areas for sampling.
Sato et al. [4] have
reported a mean sensitivity of 74% for percutaneous transhepatic
cholangioscopy-guided biopsy for revealing bile duct carcinoma in a single
specimen. They recommended that multiple biopsies be taken. The mean number of
specimens obtained in their study was 2.4, improving the sensitivity to 96%.
The guidelines for percutaneous transhepatic cholangioscopy-guided biopsy have
been reported by Tamada et al.
[5]. When cholangiography shows
a polypoid tumor, two target biopsies are sufficient. In patients with a
stenotic-type bile duct cancer in whom cholangioscopy shows a tortuous dilated
tumor vessel, two biopsies should be performed from the area of vessel.
According to the report [5], in
patients with a stenotic-type bile duct cancer in whom cholangioscopy does not
show a dilated vessel, cancer cells are present only in one small area at the
margin of the stenosis in some patients. In these patients, multiple biopsies
from the circumference of the margin of the stenotic area are important to
reduce the rate of false-negatives
[5]. These results emphasize
the importance of guidelines according to the type of tumor. In endoscopic
sonography-guided fine-needle aspiration for pancreatic malignancies, it has
been recommended that radiologists perform three to five needle passes to
ensure that an adequate sample is obtained
[32]. The sensitivity of
fluoroscopically directed biopsy obtained via the transpapillary route has
been reported to be 30-88% for bile duct carcinoma and 37-71% for pancreatic
cancer
[6,7,8].
Triple-tissue sampling improves the sensitivity
[8]. To our knowledge, the
number of biopsies required for adequate sampling in performing percutaneous
transhepatic intraluminal forceps biopsy with fluoroscopic guidance has not
been investigated.
On the basis of the current study, we propose the following guidelines for
performing biopsies. When cholangiography shows a polypoid lesion, two
biopsies are sufficient. When cholangiography shows a stenotic lesion,
performing as many as nine biopsies improves sensitivity. When patients
undergo intraductal sonography that shows a circular lesion, three biopsies
are sufficient. When intraductal sonography shows a semicircular lesion,
obtaining three to nine biopsy specimens improves diagnostic sensitivity. Of
course, if patients have not undergone intraductal sonography, taking multiple
specimens is recommended.
Our method is a sensitive endoluminal biopsy technique. The number of
biopsies required to make a diagnosis of carcinoma depends on the
cholangiographic and intraductal sonographic appearance of the tumor.
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Abstract
Introduction
