Sonographic Diagnosis of Biliary

Atresia in Pediatric Patients

Downloaded from www.ajronline.org by 202.152.205.66 on 06/12/13 from IP address 202.152.205.66. Copyright ARRS. For personal use only; all rights reserved

Using the Triangular Cord Sign

Versus Gallbladder Length and
Contraction
Kimio Kanegawa1 OBJECTIVE. A retrospective review was performed to evaluate the importance of the
Yoshinobu Akasaka1 triangular cord sign in comparison with gallbladder length and contraction for the diagnosis
Eri Kitamura1 of biliary atresia in pediatric patients.
Syoji Nishiyama1 MATERIALS AND METHODS. Fifty-five fasting infants with cholestatic jaundice
were examined on sonography. The examinations focused on the visualization of the triangu-
Toshihiro Muraji2
lar cord sign and assessment of gallbladder length and contraction. The diagnosis of neonatal
Eiji Nishijima2
hepatitis or of other causes of infantile cholestasis was made if symptom resolution occurred
Shiiki Satoh2 during follow-up.
Chikara Tsugawa2 RESULTS. A triangular cord sign was found in 27 of 29 infants with biliary atresia and in
one of 26 infants with neonatal hepatitis or other causes of infantile cholestasis. The diagnos-
tic accuracy was 95%, sensitivity was 93%, and specificity was 96%. The gallbladder was
thought to be abnormal if it was less than 1.5 cm long, was not detectable, or was detectable
but had no lumen. The gallbladder was abnormal in 21 of 29 infants with biliary atresia,
whereas it was abnormal in eight of 26 infants with neonatal hepatitis or other causes of infan-
tile cholestasis. The diagnostic accuracy was 71%, sensitivity was 72%, and specificity was
69%. The gallbladder was detectable on sonography in 13 infants with biliary atresia and 26
infants with neonatal hepatitis or other causes of infantile cholestasis. Gallbladder contraction
was not confirmed in 11 of 13 infants with biliary atresia and seven of 26 infants with neona-
tal hepatitis or other causes of infantile cholestasis. The diagnostic accuracy was 77%, sensi-
tivity was 85%, and specificity was 73%.
CONCLUSION. The triangular cord sign was a more useful sonographic finding for di-
agnosing biliary atresia than gallbladder length and contraction.

E arly diagnosis of biliary atresia is

Received March 7, 2003; accepted after revision
May 14, 2003.
1Department of Radiology, Kobe Childrens Hospital,
1-1-1 Takakuradai Suma-ku, Kobe 654-0081, Japan.
Address correspondence to K. Kanegawa.
2
Department of Pediatric Surgery, Kobe Childrens
Hospital, Kobe 654-0081, Japan.
AJR 2003;181:13871390
0361803X/03/18151387
American Roentgen Ray Society
important for achieving a favor-
able outcome. If the Kasai opera-
tion is performed within the first 2 months of
life, more than 60% of infants will achieve
jaundice-free survival [1]. Thus, differentiation
of biliary atresia from neonatal hepatitis or
other causes of infantile cholestatic jaundice is
important; however, making a definitive diag-
nosis is difficult with any of the available diag-
nostic procedures, including hepatobiliary
scintigraphy, sonography, and percutaneous
liver biopsy [13]. Sonography has long
played a role in screening infants with
cholestasis, with examinations focusing
mainly on the length and contractility of the
gallbladder [1, 2, 4]. In 1996, Choi et al. [5] re-
ported a new sonographic finding: a triangular
or tubular structure composed of fibrous tissue
located cranial to the portal vein bifurcation.
These researchers named the finding the tri-
angular cord sign. They concluded that detec-
tion of the triangular cord sign is a useful
finding for the diagnosis of biliary atresia.
Subsequent reports [68] and other studies [9,
10] support this conclusion.
The aim of the present study was to evaluate
the importance of the sonographic finding of
the triangular cord sign relative to gallbladder
length and gallbladder contraction in the diag-
nosis of biliary atresia in pediatric patients.
Materials and Methods
Fifty-five infants with cholestatic jaundice under-
went sonography from June 1996 to December
2002. Their ages ranged from 8 to 144 days (mean,
53.6 days), and the symptoms were jaundice (conju-

AJR:181, November 2003 1387


Downloaded from www.ajronline.org by 202.152.205.66 on 06/12/13 from IP address 202.152.205.66. Copyright ARRS. For personal use only; all rights reserved
Fig. 1.Sonogram illustrates method of measuring
gallbladder length (long arrow) and width (short ar-
row). These measurements were obtained using max-
imal longitudinal image.
gated hyperbilirubinemia) and acholic stools or ei-
ther symptom alone. Infants with choledochal cysts
and those with a gallbladder stone were excluded
from this study.
Sonography was performed by two of the authors
either using an SSD 500 sonographic machine
(Aloka, Tokyo, Japan) and a 5-MHz convex trans-
ducer or a 7.5-MHz linear transducer or using a
LOGIQ 500 sonographic machine (General Electric
Medical Systems, Milwaukee, WI) and an 8.2-MHz
linear transducer. All infants fasted for at least 3 hr
before the examination but were allowed to drink
milk during the procedure. The examination focused
on visualization of the triangular cord and on assess-
ment of the length and contraction of the gallbladder.
The length and width of the gallbladder were mea-
sured on the maximal longitudinal image (Fig. 1). For
A B
Fig. 3.95-day-old female infant with neonatal hepatitis.
A, Sonogram shows normal gallbladder. Gallbladder is 3.1 cm long.
B, Sonogram obtained 1 hr after patient was fed shows gallbladder is contracted. Contraction index was 99.6%.
1388
Kanegawa et al.
Fig. 2.35-day-old male infant with biliary atresia.
Sonogram reveals tubular echogenic cord (arrows).
evaluation of gallbladder contraction, the examination
was repeated 6090 min after the infant was fed.
As described in previous reports [1, 68], the
triangular cord was defined as a triangular- or tubu-
lar-shaped echogenic density that was located im-
mediately cranial to the portal vein bifurcation and
was 3 mm or more thick (Fig. 2). Detection of the
triangular cord sign was defined as indicative of
biliary atresia, and the absence of the triangular
cord sign was interpreted as indicative of neonatal
hepatitis or other causes of infantile cholestasis.
The gallbladder was thought to be normal if it was
1.5 cm or more long (Fig. 3A); the gallbladder was
considered abnormal if it was less than 1.5 cm
long, was not detectable, or was detectable but had
no lumen (Fig. 4A). An abnormal gallbladder is
thought to be more suggestive of biliary atresia
than of neonatal hepatitis or other causes of infan-
tile cholestasis [7]. Gallbladder contraction was
evaluated by calculating the contraction index (CI)
as follows:
(fasting volume postprandial volume)
CI (%) = 100
fasting volume
The volume of the gallbladder was calculated
using the following equation [12]:
0.52 width width length.
A normal contraction index was reported to be
86% 18% (mean SD) in 6-week-old infants
and 67% 42% in 4-month-old infants [12]. Be-
cause the normal range of the contraction index
has been reported only in 6-week-old infants and
4-month-old infants, we used the 6-week value for
patients younger than 12 weeks old and the 4-
month value for patients 12 weeks old or older. If
the contraction index was less than the mean SD,
the gallbladder was described as uncontracted
(Figs. 3 and 4). An uncontracted gallbladder was
thought to be more suggestive of biliary atresia
than of neonatal hepatitis or other causes of infan-
tile cholestasis.
The diagnosis of biliary atresia was confirmed
at surgery, and the diagnosis of neonatal hepatitis
or of other types of infantile cholestasis was con-
firmed by the resolution of symptoms on follow-
up. Of 55 infants, 29 had biliary atresia, two had
Alagille syndrome, and 24 had neonatal hepatitis
or other causes of infantile cholestasis.
Results
Triangular Cord Sign
Among the 29 infants with biliary atresia,
sonography showed the triangular cord sign in
27 patients, but the triangular cord sign was
not seen on sonography in two patients. In
these two infants with biliary atresia in whom
the triangular cord sign was not visible, the
gallbladder was not visualized. The triangular
cord sign was not found on sonography in 25
of 26 infants with neonatal hepatitis or other
causes of infantile cholestasis. The remaining
infant who showed a triangular cord (Fig. 5)
but did not have biliary atresia underwent se-
rial sonographic examination at the ages of 37
and 50 days. The triangular cord sign was seen
on each examination, and it was 0.30.4 cm
wide and 1.31.6 cm long. In this infant, jaun-
dice was no longer present when the infant
was 90 days old. The diagnostic accuracy of
the triangular cord sign was 95%, sensitivity
was 93%, and specificity was 96%.
AJR:181, November 2003

Downloaded from www.ajronline.org by 202.152.205.66 on 06/12/13 from IP address 202.152.205.66. Copyright ARRS. For personal use only; all rights reserved
A B
Fig. 4.64-day-old female infant with biliary atresia.
A, Sonogram shows abnormal gallbladder (arrows). Gallbladder is 1.0 cm long.
B, Sonogram obtained 1 hr after patient was fed shows that gallbladder (arrows) has not contracted. Contraction
index was 0%.
Gallbladder Length
Among the 29 infants with biliary atresia, the
gallbladder was considered abnormal in 21 and
normal in eight. In 16 of the 21 infants with an
abnormal gallbladder, the gallbladder was not
detectable or was detected but had no lumen. In
the other five infants, the gallbladder was less
than 1.5 cm long. Among the 26 infants with
neonatal hepatitis or other causes of infantile
cholestasis, the gallbladder was abnormal in
eight and normal in 18. The diagnostic accuracy
of gallbladder length was 71%, sensitivity was
72%, and specificity was 69%.
Gallbladder Contraction
In 11 of 13 infants with biliary atresia and a
detectable gallbladder, contraction was not
seen. Gallbladder contraction was confirmed
in only two infants with biliary atresia. In
seven of the 26 infants with neonatal hepatitis
or other causes of infantile cholestasis, gall-
bladder contraction was not seen, and in the re-
maining 19 infants in this group, gallbladder
contraction was detected. The diagnostic accu-
racy of gallbladder contraction was 77%, sen-
sitivity was 85%, and specificity was 73%.
Discussion
The cause of biliary atresia is still unknown.
Unless the Kasai operation is performed
within the first 2 months of life, survival with-
out portal hypertension is unlikely; therefore,
accurate and prompt diagnosis is important for
early treatment. However, distinguishing bil-
iary atresia from neonatal hepatitis or other
causes of infantile cholestasis is sometimes
AJR:181, November 2003
Sonographic Diagnosis of Biliary Atresia
Fig. 5.15-day-old female neonate with unknown
difficult with any of the clinically available
methods. Hepatobiliary scintigraphy has been
used for this purpose. If the radiotracer is ex-
creted into the gastrointestinal tract, biliary
atresia can be excluded. However, failure to
excrete the radiotracer occurs in both neonatal
hepatitis and biliary atresia, so the specificity
of this method is not adequate.
Sonography is a simple and noninvasive
method for evaluating cholestasis in infants. Oc-
casionally, sonography detects other causes of
infantile cholestasis such as a choledochal cyst.
Performing sonography after the administration
of phenobarbital is useful because phenobar-
bital enhances bile flow and improves the de-
tectability of the gallbladder in severe neonatal
hepatitis [4]. In the past, sonography was fo-
cused on the assessment of the length, contrac-
tility, or both of the gallbladder in fasting infants
to distinguish biliary atresia from neonatal hep-
atitis. A small or undetectable gallbladder and
the absence of gallbladder contraction were
thought to be suggestive of biliary atresia. How-
ever, a small gallbladder or an uncontracted
gallbladder may be seen both in biliary atresia
and in neonatal hepatitis [3]. Furthermore, re-
ports indicate that some patients with biliary
atresia have a normal gallbladder [3, 7]. A gall-
bladder that is less than 1.5 cm long is sugges-
tive of biliary atresia [2, 3], but biliary atresia
associated with a gallbladder longer than 1.5 cm
has been reported [7]. Based on the results of
our series, the size of the gallbladder does not
seem to be a decisive finding for the diagnosis
of biliary atresia.
Contraction of the gallbladder has also been
reported in patients with biliary atresia [12,
cause of infantile cholestasis. Sonogram reveals tu-
bular echogenic cord (arrows). Triangular cord was
0.30.4 cm wide and 1.31.6 cm long.
13]. One study showed that gallbladder con-
traction occurs in 920% of infants with bil-
iary atresia [12], but the method of evaluating
gallbladder contraction in that study is unclear.
We adapted the contraction index and the nor-
mal ranges reported by Weinberger et al. [11].
Because these researchers reported contraction
index data in 6-week-old and 4-month-old in-
fants, we used the normal range for 6-week-
old infants for patients younger than 12 weeks
old and the normal range for 4-month-old in-
fants for patients 12 weeks old or older. In our
series, gallbladder contraction was not a satis-
factory diagnostic sign. Gallbladder contrac-
tion was observed in two patients with biliary
atresia in this series. In these patients, the mor-
phologic type of porta hepatis was type IIIa
and type IIIb of the Kasai classification [1].
Gallbladder contraction was previously re-
ported to occur in patients with type IIIa porta
hepatis [11, 12], in which the common bile
duct is patent. In a patient with type IIIb porta
hepatis, the common bile duct was microscopi-
cally measured as 50300 m; therefore, the
mechanism of contraction is unclear.
Choi et al. [5] and Park et al. [68] reported a
sonographic finding that they named the trian-
gular cord sign, which was a triangular- or tu-
bular mass of fibrous tissue cranial to the portal
vein bifurcation. Because of the high sensitivity,
specificity, and diagnostic accuracy of this find-
ing, these researchers concluded that the trian-
gular cord sign was a useful sonographic
finding for the diagnosis of biliary atresia. The
triangular cord is thought to be the fibrous rem-
nant of the duct in infants with biliary atresia.
Park et al. [7] reported that the diagnostic accu-
1389

racy, specificity, and sensitivity of the triangular
cord sign was 93%, 83%, and 98%, respec-
tively. The results of our study were similar to
their findings. Two infants with biliary atresia in
our series did not have a triangular cord: one
had scanty fibrous tissue at surgery, and the
Downloaded from www.ajronline.org by 202.152.205.66 on 06/12/13 from IP address 202.152.205.66. Copyright ARRS. For personal use only; all rights reserved
other had virtually no fibrous tissue. Ohi [1] re-
ported that the incidence of fibrous tissue at sur-
gery was 67% in patients with biliary atresia,
which would indicate that 33% of these patients
had no triangular cord. However, our results and
those of others show a higher incidence of the
triangular cord in patients with biliary atresia
(8393%) than Ohi reported. In our series, there
was one false-positive finding of triangular
cord. Another such patient was reported previ-
ously, and the cause of the false-positive finding
was thought to be periportal edema or thicken-
ing [7]. In our patient with the false-positive
finding, follow-up sonography was performed
twice and the triangular cord sign was seen at
each examination. The gallbladder was consid-
ered abnormal because it was less than 1.5 cm
long and contraction was negative. This patient
had trisomy 13 syndrome and experienced car-
diac dysfunction, but jaundice resolved sponta-
neously after 2 months. The cause of the false-
positive finding is unknown, but periportal
1390
Kanegawa et al.
edema may have led to the detection of the tri-
angular cord sign.
In conclusion, the diagnostic accuracy, speci-
ficity, and sensitivity of the triangular cord sign
are superior to those of gallbladder length and
gallbladder contraction, so the triangular cord
sign seems to be the a more useful sonographic
finding for making a diagnosis of biliary atresia
than gallbladder length and contraction.
References
1. Ohi R. Biliary atresia. In: Balistreri WF, Ohi R,
Todani T, Tuscida Y, eds. Hepatobiliary pancre-
atic and splenic disease in children, 1st ed. Am-
sterdam: Elsevier, 1997:231260
2. Abramson SJ, Treves S, Teele RL. The infant
with possible biliary atresia: evaluation by ultra-
sound and nuclear medicine. Pediatr Radiol
1982;12:15
3. Kirks DR, Coleman RE, Filston HC, Rosenberg
ER, Merten DF. An imaging approach to persis-
tent neonatal jaundice. AJR 1984;142:461465
4. Ikeda S, Sere Y, Yamamoto H, Ogawa M. Effect
of phenobarbital on serial ultrasonic examination
in the evaluation of neonatal jaundice. Clin Imag-
ing 1994;18:146148
5. Choi SO, Park WH, Lee HJ, Woo SK. Triangular
cord: a sonographic finding applicable in the di-
agnosis of biliary atresia. J Pediatr Surg 1996;
31:363366
6. Park WH, Choi SO, Lee HJ, Kim SP, Zeon SK
Lee SK. A new diagnostic approach to biliary
atresia with emphasis on the ultrasonographic tri-
angular cord sign: comparison of ultrasonogra-
phy, hepatobiliary scintigraphy, and liver needle
biopsy in the evaluation of infantile cholestasis. J
Pediatr Surg 1997;32:15551559
7. Park WH, Choi SO, Lee HJ. The ultrasonographic
triangular cord coupled with gallbladder im-
ages in diagnostic prediction of biliary atresia
from infantile intrahepatic cholestasis. J Pediatr
Surg 1999;34:17061710
8. Park WH, Choi SO, Lee HJ. Technical innovation
for noninvasive and early diagnosis of biliary atre-
sia: the ultrasonographic triangular cord sign. J
Hepatobiliary Pancreat Surg 2001;8:337341
9. Kendric APT, Phua KB, Subramaniam R, Goh
ASW, Ooi BC, Tan CE. Making the diagnosis of
biliary atresia using the triangular cord sign and
gallbladder length. Pediatr Radiol 2000;30:6973
10. Kotb MA, Kotb A, Sheba MF, et al. Evaluation of
the triangular cord sign in the diagnosis of biliary
atresia. Pediatrics 2001;108:416420
11. Weinberger E, Blumhagen JD, Odell JM. Gall-
bladder contraction in biliary atresia. AJR
1987;149:401402
12. Ikeda S, Sere Y, Ohshiro H, Uchino S, Akizuki M,
Kondo Y. Gallbladder contraction in biliary atre-
sia: a pitfall of ultrasound diagnosis. Pediatr Ra-
diol 1998;28:451453
13. Lehtonen L, Svedstrom E, Korvenranta H. The
size and contractility of the gallbladder in infants.
Pediatr Radiol 1992;22:515518
AJR:181, November 2003