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DOI: 10.1148/radiol.292020472
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(Radiology 2003;229:395-400.)
© RSNA, 2003

Pediatric Imaging

Objective Criteria of Triangular Cord Sign in Biliary Atresia on US Scans1

Hee-Jung Lee, MD, Sung-Moon Lee, MD, Woo-Hyun Park, MD and Soon-Ok Choi, MD

1 From the Departments of Diagnostic Radiology (H.J.L., S.M.L.) and Pediatric Surgery (W.H.P., S.O.C.), School of Medicine & Institute for Medical Science, Keimyung University Dongsan Medical Center, 196 Dongsandong, Chunggu, Taegu 700–310, Korea. Received April 22, 2002; revision requested June 21; final revision received February 26, 2003; accepted March 20. Supported by the research promoting grant from the Keimyung University Dongsan Medical Center in 2001. Address correspondence to H.J.L. (e-mail: hjlee@dsmc.or.kr).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To develop objective criteria for the ultrasonographic (US) appearance of the triangular cord (TC) sign for the diagnosis of biliary atresia.

MATERIALS AND METHODS: US was performed in 86 infants with jaundice. Biliary atresia (n = 20) was confirmed with hepatoportoenterostomy. Neonatal hepatitis (n = 66) was diagnosed with needle biopsy (n = 5), cholescintigraphy (n = 19), or clinical findings (n = 42). Thickness of the echogenic anterior wall of the right portal vein (EARPV) was measured. The TC sign was defined as thickness of the EARPV of more than 4 mm on a longitudinal scan. Biliary atresia was diagnosed when the TC sign was present. Statistical analyses were performed to compare the thickness of the EARPV between patients with biliary atresia and those with neonatal hepatitis and to test the significance of a 4-mm thickness as the criterion for the TC sign in the differentiation of biliary atresia from neonatal hepatitis (P < .05).

RESULTS: The TC sign was present in 16 (80%) of 20 patients with biliary atresia and in one of 66 patients with neonatal hepatitis. Mean thickness of the EARPV was significantly greater in patients with biliary atresia (5.39 mm) than in patients with neonatal hepatitis (2.17 mm) (P < .05). Use of 4-mm thickness as the criterion for TC sign was statistically significant (P < .05), resulting in a sensitivity of 80%, specificity of 98%, and positive and negative predictive values of 94% for the diagnosis of biliary atresia.

CONCLUSION: An objective criterion of the TC sign is an EARPV thicker than 4 mm on a longitudinal scan.

© RSNA, 2003

Index terms: Bile ducts, diseases, 768.1434 • Bile ducts, US, 768.1298 • Infants, newborn, gastrointestinal tract, 768.1434 • Portal vein, abnormalities, 957.1434 • Portal vein, US, 957.1298


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Although the pathogenesis of biliary atresia is still unknown, the disease is characterized by luminal obstruction of the extrahepatic bile duct with a fibrous ductal remnant, which represents the obliterated ductal remnant in the porta hepatis at surgery (Fig 1) (1,2). To our knowledge, we were the first to report the triangular cord (TC) sign to demonstrate this obliterated fibrous ductal remnant in the porta hepatis by using ultrasonography (US) (3). According to our original description, the TC sign was defined as the presence of an abnormal triangular or tubular echogenic area in the region of the porta hepatis on a transverse or longitidinal US scan. Several investigators have described the TC sign as a useful and specific US finding for the differential diagnosis of biliary atresia from neonatal hepatitis (4,5).



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  		Figure 1a. Surgical findings of biliary atresia. (a) Photograph of surgical specimen of obliterated extrahepatic bile ducts shows the fibrous ductal remnant (black arrowheads) in the porta hepatis, atretic gallbladder (arrow), and fibrous common bile duct (white arrowhead). The fibrous ductal remnant is a triangular cone-shaped mass. (b) Schematic drawing represents the anatomic relationship between the fibrous ductal remnant and blood vessels around the porta hepatis. The triangular, cone-shaped, fibrous ductal remnant (black arrowheads, green) is positioned anterior and slightly superior to the portal vein (long arrow, blue) and the hepatic artery (short arrow, red).

 


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  		Figure 1b. Surgical findings of biliary atresia. (a) Photograph of surgical specimen of obliterated extrahepatic bile ducts shows the fibrous ductal remnant (black arrowheads) in the porta hepatis, atretic gallbladder (arrow), and fibrous common bile duct (white arrowhead). The fibrous ductal remnant is a triangular cone-shaped mass. (b) Schematic drawing represents the anatomic relationship between the fibrous ductal remnant and blood vessels around the porta hepatis. The triangular, cone-shaped, fibrous ductal remnant (black arrowheads, green) is positioned anterior and slightly superior to the portal vein (long arrow, blue) and the hepatic artery (short arrow, red).

 
US is an operator-dependent modality, however, and there can be controversy over the precise definition of the abnormal echogenic area in the porta hepatis. We have stressed the fact that a study designed to define abnormal triangular or tubular echogenicity is fundamental to accurately describe the TC sign. Since our original study, we have been impressed and encouraged by the idea that the TC sign can be objectively measured with US; therefore, the purpose of the present study was to develop objective criteria for the US appearance of the TC sign for the diagnosis of biliary atresia.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
From January 1998 to December 2001, 151 consecutive infants with persistent neonatal jaundice underwent hepatobiliary US. Among them, 48 patients with unconjugated hyperbilirubinemia related to prematurity with or without total parenteral nutrition (n = 42), hemolysis (n = 3), or breast-feeding (n = 3) were excluded. Three infants with a choledochal cyst were excluded from the study. Fourteen infants were lost to follow-up and were also excluded. As a result, 86 infants with conjugated hyperbilirubinemia and confirmed biliary atresia or neonatal hepatitis were enrolled in this study. Eighty-four infants were younger than 4 months, (range, 5–120 days; mean, 50 days), and two were 7 months old. The study was approved by our institutional medical ethical review board. Informed consent was obtained from parents before the examination.

Biliary atresia was diagnosed in 20 infants (13 girls and seven boys) aged 5–210 days (mean, 66 days). Neonatal hepatitis was diagnosed in 66 infants (46 boys and 20 girls) aged 6–210 days (mean, 50 days). Biliary atresia was confirmed with surgery and wedge liver biopsy in all 20 infants. Neonatal hepatitis was confirmed with percutaneous needle aspiration biopsy (n = 5), cholescintigraphy (n = 19), or clinical findings (n = 42). Clinical findings of neonatal hepatitis were verified by the patient’s recovery from jaundice and the normalization of laboratory values during a clinical follow-up period, which lasted from 2 weeks to 4 months.

Imaging
All US examinations were performed by the primary author (H.J.L.). Commercially available real-time units (Sequoia 512, Acuson, Mountain View, Calif; DHI 5000, Advanced Technology Laboratories, Bothell, Wash) with 6–8-MHz convex and 8–15-MHz linear transducers were used. Infants fasted for 4 hours in preparation for the general abdominal screening examination. In addition to routine scanning of the solid organs of the upper abdomen, we paid special attention to the porta hepatis by using a linear-array transducer of more than 8 MHz.

The thickness of the echogenic anterior wall of the right portal vein (EARPV) was measured. The sole criterion for the TC sign in this study was an EARPV thickness of more than 4 mm on a longitudinal scan (Fig 2). A thickness of 4 mm was chosen as the upper limit for all normal possible structures that could be positioned along the anterior aspect of the right portal vein, including the anterior wall of the right portal vein (1 mm), anterior wall of the right hepatic artery (1 mm), and the common hepatic duct (1–2 mm). For consistency, measurements were obtained in the proximal portion of the right portal vein just before anterior and posterior divisions. If both the right portal vein and the right hepatic artery were identified on the same scan, the lumen and both the anterior and posterior walls of the right hepatic artery were also measured. Measurement was made from the inner to the outer wall and perpendicular to the plane of the scan. When the echogenic wall was not of uniform thickness, the greatest thickness was used, as relevant for the study. To calculate the average thickness of walls that were very faint, those less than 1 mm thick were arbitrarily assigned a thickness of 1 mm. The investigating radiologist (H.J.L.) obtained this measurement during the US examination by using electronic calipers.



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  		Figure 2. Depiction of TC sign. The EARPV was 5.4 mm thick on this longitudinal US scan, which shows the TC sign (cursors) as a thick, tubular, echogenic area along the anterior aspect of the right portal vein (long arrow). The right hepatic artery (short arrow) is encased within the EARPV.

 
Image Analysis
All US scans were interpreted independently by two radiologists who were experienced in gastrointestinal US and were blinded to the clinical history of the patients. Images were reviewed for the presence or absence of the TC sign. The diagnosis of biliary atresia was made when the TC sign was present on US scans. All patients with biliary atresia underwent hepatoportoenterostomy within 7–10 days of US examination, and the fibrous ductal remnants were removed from the porta hepatis at surgery. US findings were compared with surgical findings.

Data Analysis
To describe the thickness of the EARPV, baseline characteristics are presented as range, mean, and SD. The Mann-Whitney rank sum test was used to evaluate statistically significant differences in the mean thicknesses of the EARPV in patients with biliary atresia and those with neonatal hepatitis. We performed a separate Mann-Whitney test in which we excluded patients who were cared for as though they had a 1-mm-thick EARPV. The Fisher exact test was used to test the significance of a 4-mm thickness as the criterion for the TC sign in the differentiation of biliary atresia from neonatal hepatitis. We also evaluated the diagnostic value of the TC sign by using a 4-mm thickness as the criterion. A P value of less than .05 was considered to indicate a statistically significant difference. Data analyses were performed with a statistical software package (SPSS version 10; SPSS, Chicago, Ill) for Windows (Microsoft, Redmond, Wash).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
On the basis of the criterion used for the TC sign, biliary atresia was diagnosed in 17 patients, including 16 with biliary atresia (Fig 3a) and one with neonatal hepatitis. The scans of 65 of 66 patients with neonatal hepatitis did not show the TC sign (Fig 4). There was no disagreement about interpretation of the TC sign between the two radiologists who reviewed the images. In all 16 patients with biliary atresia whose scans showed the TC sign, surgery revealed a fibrous ductal remnant of a triangular, cone-shaped fibrous mass along the anterior aspect of the portal vein and hepatic artery. In two of the four patients with biliary atresia whose US scans did not depict the TC sign, surgery showed a fibrous ductal remnant of a fibrous hepatic duct (Fig 5). The remaining two patients both had a relatively small, triangular, cone-shaped, fibrous mass in the porta hepatis.



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  		Figure 3a. US images of a 35-day-old boy with biliary atresia. (a) Longitudinal scan shows TC sign (cursors) with a 5.1-mm-thick EARPV. (b) Transverse scan shows triangular echogenic area (cursors) in the anterior aspect of the portal vein in the porta hepatis.

 


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  		Figure 3b. US images of a 35-day-old boy with biliary atresia. (a) Longitudinal scan shows TC sign (cursors) with a 5.1-mm-thick EARPV. (b) Transverse scan shows triangular echogenic area (cursors) in the anterior aspect of the portal vein in the porta hepatis.

 


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  		Figure 4. US image of a 36-day-old boy with neonatal hepatitis. Longitudinal scan shows no demonstrable TC sign (cursors). The EARPV is 1.5 mm thick between cursors.

 


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  		Figure 5a. Images of a 36-day-old boy with biliary atresia but no demonstrable TC sign. (a) Longitudinal US scan shows EARPV is 3.0 mm thick between cursors. (b) Surgical specimen of the fibrous ductal remnant is a pattern of fibrous hepatic duct (arrowheads) in the porta hepatis.

 


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  		Figure 5b. Images of a 36-day-old boy with biliary atresia but no demonstrable TC sign. (a) Longitudinal US scan shows EARPV is 3.0 mm thick between cursors. (b) Surgical specimen of the fibrous ductal remnant is a pattern of fibrous hepatic duct (arrowheads) in the porta hepatis.

 
One patient who had neonatal hepatitis with the TC sign did not have bowel activity during a 24-hour period, as depicted by cholescintigraphy. The findings of needle aspiration biopsy demonstrated equivocal histopathologic findings of both biliary atresia and neonatal hepatitis with giant cell transformation, canalicular and cellular bile stasis, and cellular infiltration. Repeat biopsy was recommended, since the biopsy specimen did not contain the interlobular space. The parents refused a second biopsy and laparotomy. The diagnosis of neonatal hepatitis was verified by the patient’s recovery from jaundice with phenobarbital treatment during a hospital stay of 3 weeks.

The ranges, mean values, and SDs of the thicknesses of the EARPV are shown in the Table. There was a statistically significant difference in the thickness of the EARPV between patients with biliary atresia and those with neonatal hepatitis (P < .05). The distribution of the wall thicknesses of all 86 patients is shown in Figure 6. There were seven patients with neonatal hepatitis whose scans showed a very faint wall, and they were considered to have a wall thickness of 1 mm. A separate Mann-Whitney test performed for the remaining 79 patients revealed a statistically significant difference between the two groups (P < .05). The results of our study show that the thickness of the EARPV was greater than 4 mm in 16 of 20 patients with biliary atresia and in only one of 66 patients with neonatal hepatitis (Fisher exact test, P < .05). Use of a 4-mm thickness as a criterion for the TC sign in the diagnosis of biliary atresia resulted in a sensitivity of 80% (16 of 20), a specificity of 98% (65 of 66), a positive predictive value of 94% (16 of 17), a negative predictive value of 94% (65 of 69), and an accuracy of 94% (81 of 86).


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  		Thickness of EARPV in Patients with Biliary Atresia and in Those with Neonatal Hepatitis

 


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  		Figure 6. Scattergram shows the thickness of the EARPV in patients with biliary atresia and neonatal hepatitis. The difference in thickness was statistically significant between patients with biliary atresia and those with neonatal hepatitis. Dotted line indicates the 4-mm thickness as the criterion for the TC sign. Solid lines represent mean thickness in the groups. A single point in the scattergram is used to indicate the seven patients with a 1-mm-thick EARPV.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
US plays a major role in the evaluation of infants with cholestatic jaundice and in the differentiation of biliary atresia from neonatal hepatitis, which are the two major causes of conjugated hyperbilirubinemia in neonates and infants. Several studies have found that magnetic resonance (MR) cholangiography may also provide information that is useful in the evaluation of the patency of the intra- and extrahepatic biliary duct (6–9). MR cholangiography, however, still has limitations, including the spatial resolution related to small body size, the motion artifact induced by inadequate sedation or respiration, and cost (9). Recent advances in higher frequency transducers have revolutionized the US work-up of more detailed anatomic landmarks. Moreover, US, which is noninvasive and nonionizing and is less expensive and produces images in real time, is still an important tool in the evaluation of the hepatobiliary tree, especially in neonates and infants, who are smaller and require complete sedation for MR imaging.

Biliary atresia is characterized by fibrous obliteration of the extrahepatic bile duct with fibrous ductal remnant in the porta hepatis (2). The hepatic ducts transform into a fibrous ductal remnant that is usually anterior and slightly cranial to the hepatic artery and the portal vein. The fibrous ductal remnant takes the same course as the common hepatic duct and smoothly tapers proximally along both sides of the intrahepatic ducts (Fig 1b). Thus, the location of the fibrous ductal remnant in the porta hepatis should be the same as that of the common hepatic duct. The original definition of the TC sign was based on the idea that this fibrous ductal remnant could be seen as a thick tubular or triangular echogenic density along the anterior aspect of the portal vein (3).

The common hepatic duct should measure less than 1 mm in neonates and less than 2 mm in infants (10,11). Although criteria for the wall thickness of the normal portal vein and hepatic artery have not been established in neonates and infants, for the purposes of this study we presumed that they are less than 1 mm thick. This is the reason we choose an EARPV thickness of 4 mm as the criterion for the TC sign, which represents the thickness of normal possible structures that are positioned along the anterior aspect of the portal vein, including the anterior wall of the right portal vein, the anterior wall of the right hepatic artery, and the common hepatic duct.

The anatomic location of the bile ducts relative to the hepatic artery and the portal vein tend to be more consistent in the right lobe of the liver (12,13). This is the reason we choose this side for measurement.

The surgical morphologic finding of a fibrous ductal remnant was classified into several types, according to the pattern of the hepatic radicles at the porta hepatis, as follows: triangular, cone-shaped, fibrous mass (67%); fibrous hepatic ducts (15%); aplasia of hepatic ducts (6%); dilated hepatic ducts (5%); hypoplastic hepatic ducts (4%); and bile lake (3%) (14). Ohi and Ibrahim (14) reported that a triangular, cone-shaped, fibrous mass was the most common pattern and that this accounted for about 67% of morphologic findings. In our study, 18 (90%) of 20 patients with biliary atresia had a triangular, cone-shaped, fibrous mass and two (10%) had fibrous hepatic ducts.

Depending on the plane of imaging used for US, the triangular, cone-shaped fibrous mass can appear to have either a triangular or tubular echogenic density. In the ideal situation, the triangular, cone-shaped, fibrous mass appears as a triangular echogenic density in the porta hepatis on the transverse scan (Fig 3b). That is the reason we proposed the term triangular cord in the original description. Since the fibrous mass is oriented in the oblique coronal direction, however, there is a greater chance of an off-axis depiction. Moreover, triangular echogenic density is hard to measure exactly on a transverse scan because of errors related to its tapering structure into the liver. Also, the fibrous ductal remnant may not be in the pattern of a triangular, cone-shaped fibrous mass. Other patterns of the fibrous ductal remnant do not appear as triangular echogenic density, even on a transverse scan; therefore, the oblique longitudinal scan is potentially a more consistent and accurate way to measure the thickness of the TC sign, regardless of the patterns of fibrous ductal remnant in the porta hepatis. For these reasons, we used a longitudinal scan rather than a transverse scan for measurement.

Our data indicate the EARPV in patients with biliary atresia is thicker than the EARPV in patients with neonatal hepatitis and that this difference is statistically significant. Our results also indicate that use of a 4-mm thickness as the criterion for the TC sign offers a reliable discriminator for the differentiation between biliary atresia and neonatal hepatitis. In this study, if US depicted the TC sign in a young infant with persistent conjugated hyperbilirubinemia, biliary atresia was indicated with a positive predictive value of 94%. If the patient had no demonstrable TC sign, neonatal hepatitis was indicated with a negative predictive value of 94%. The TC sign, therefore, can reliably lead to the exclusion or confirmation of the presence of biliary atresia.

There is a little overlap in the thickness of the EARPV of biliary atresia and neonatal hepatitis, as shown in Figure 6, and this overlap results in certain limitations. Unfortunately, the US scans of four patients with biliary atresia did not depict the TC sign. The ability of physicians to identify the TC sign with US in patients with biliary atresia depends on the patterns and size of the fibrous ductal remnant in the porta hepatis. Other patterns of the fibrous ductal remnant, such as fibrous hepatic ducts, aplasia of the hepatic ducts, dilated hepatic ducts, hypoplastic hepatic ducts, and bile lake would lead to a negative TC sign, as shown in our two patients. Although we did not correlate the size of the fibrous ducal remnant at surgery with the thickness of the TC sign, a small fibrous ductal mass, even with the pattern of triangular cone-shaped fibrous mass, also may not demonstrate the TC sign. Thus, we recommend that US examinations should be performed with a high-resolution (>8 MHz) linear probe so that even a relatively small fibrous ductal remnant will be depicted.

Any abnormal condition causing periportal infiltration, including periportal edema, fibrosis, or tumorous condition, can appear as a TC sign. Severe neonatal hepatitis with periportal fibrosis, however, would not usually be so advanced in the first several months of life. In fact, the scans of two patients with congenital leukemia and severe sepsis also depicted the TC sign. These two patients were not included in this study, however, since they were referred for evaluation of hepatomegaly with abnormal hematologic findings and not for evaluation of cholestatic jaundice. Among the 48 patients with unconjugated hyperbilirubinemia who were excluded from this study, the TC sign was depicted on the scan of one prematurely born patient with total parenteral nutrition. The conditions of these three patients were clinically suggested and diagnosed without difficulty.

In this study, we successfully measured the TC sign and proposed an objective criterion for the TC sign in the diagnosis of biliary atreisa. The present study also indicates the need for further investigation into the precise role of the TC sign as a quantitative measurement of periportal fibrosis in patients with biliary atresia.

In conclusion, we propose the TC sign be defined as a thickness of the EARPV echogenic anterior wall of the right portal vein of more than 4 mm on a longitudinal scan. The use of this criterion for the diagnosis of biliary atresia resulted in a sensitivity of 80%, a specificity of 98%, a positive predictive value of 94%, a negative predictive value of 94%, and an accuracy of 94%. The ability to identify the TC sign on US scans in patients with biliary atresia depends on the pattern and size of the fibrous ductal remnant in the porta hepatis.


   ACKNOWLEDGMENTS
 
We thank Hyun-Sook Lim, MSc Med, from the Department of Preventive Medicine, Keimyung University Dongsan Medical Center, Korea, for her advice and contribution to the statistical analysis in the present study.


   FOOTNOTES
 
Abbreviations: EARPV = echogenic anterior wall of the right portal vein, TC = triangular cord

Author contributions: Guarantor of integrity of entire study, H.J.L.; study concepts and design, H.J.L.; literature research, S.M.L.; clinical studies, W.H.P., S.O.C.; data acquisition, S.M.L., H.J.L.; data analysis/interpretation, H.J.L.; statistical analysis, H.J.L.; manuscript preparation, H.J.L., S.M.L.; manuscript definition of intellectual content, W.H.P.; manuscript editing, H.J.L., S.M.L.; manuscript revision/review, all authors; manuscript final version approval, S.M.L., W.H.P., S.O.C.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

  1. Landing BH. Consideration of the pathogenesis of neonatal hepatitis, biliary atresia and choledochal cyst: the concept of infantile obstructive cholangiopathy. Prog Pediatr Surg 1974; 6:113-139.[Medline]
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  8. Miyazaki T, Yamashita Y, Tang Y, et al. Single-shot MR cholangiopancreaticography of neonates, infants, and young children. AJR Am J Roentgenol 1998; 170:33-37.[Abstract/Free Full Text]
  9. Jaw TS, Kuo YT, Liu GC, Chen SH, Wang CK. MR cholangiography in the evaluation of neonatal cholestasis. Radiology 1999; 212:249-256.[Abstract/Free Full Text]
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