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British Journal of Radiology (2005) 78, 884-887
© 2005 British Institute of Radiology
doi: 10.1259/bjr/34728497
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Full Paper

Post-portoenterostomy triangular cord sign prognostic value in biliary atresia: a prospective study

M A Kotb, MD 1 M Sheba, MD 1 N El Koofy, MD 1 S Mansour, MD 1 H M El Karaksy, MD 1 N M Dessouki, MD 2 W Mostafa, MSc 2 M El Barbary, MD 2 H E El-Tantawy, MD 2 and S Kaddah, MD 2

Departments of 1 Paediatrics and 2 Paediatric Surgery, Cairo University, Egypt


   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 References
 
The triangular cord sign (TC sign) is a sensitive and specific tool in prompt diagnosis of extrahepatic biliary atresia. The objective of this study is to evaluate post-operative TC sign presence in outcome prediction of infants with biliary atresia after Kasai hepato-portoenterostomy 27 infants and children with biliary atresia underwent 122 ultrasound examinations using both 5 MHz and 7 MHz convex linear transducers in 33 months follow up. For all infants TC sign identification was included pre-operatively, ultrasound was done 2 weeks post-operatively then bimonthly for 3 months, monthly for 2 months and every 3 months thereafter. 14 (53.8%) had post-operative TC sign. Once post-operatively positive, it remained positive throughout the study. It did not reappear in an initially post-operatively TC sign negative infant. Those having post-operative TC sign had statistically worse outcomes (0 became anicteric, 2 improved, 7 had progressive disease and 6 died) than those with a negative TC sign (p=0.04) (3 became anicteric, 5 improved, 2 progressed and 1 died). Presence of TC sign post-operatively correlated with measure of removal of all fibrous cone at porta-hepatis during portoenterostomy (p=0.026). Post-portoenterostomy TC sign is associated with more morbidity and mortality; and reflects inadequate surgical technique.


   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 References
 
The triangular cord (TC sign), a band-like periportal echogenicity (3 mm or greater in thickness) that represents a cone shaped fibrotic mass cranial to the portal vein, was reported to be a specific ultrasound finding in the prompt diagnosis of biliary atresia. The TC sign has reported diagnostic accuracy of 84.2–95% with 85–95% sensitivity and 100% specificity [1–5].

Extrahepatic biliary atresia is characteristically a progressive obstructive cholangiopathy. Palliative surgery such as a Kasai portoenterostomy attempts to establish bile flow in biliary atresia. The success of this procedure is greatest when performed within the first 2 months of life, but it is curative only in a minority of cases [6]. More commonly, these patients have deterioration in their liver function and eventually need a liver transplant (65% to 80% of the children with biliary atresia will eventually require liver transplantation) [7–10]. Predictors of a poor outcome were reported to be Caucasian, with an operative age greater than 60 days, presence of cirrhosis on initial biopsy, totally non-patent extrahepatic ducts, and absence of ducts at the level of the liver hilum. Bile duct profiles of 150 µm or greater, lined with columnar epithelium and prehilar bile duct structures of more than 400 µm, were associated with a favourable prognosis [11, 12].

The aim of this work was to define the post-operative presence of the ultrasound TC sign and its role in the prediction of outcome of infants with biliary atresia after Kasai hepato-portoenterostomy.


   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 References
 
This study included 27 infants with extrahepatic biliary atresia who were studied prospectively starting at the time of initial diagnosis. They were attendants of the Hepatology Clinic of the New Children's Hospital, Cairo University. Parents of the participating infants gave their consent to the trial. The study commenced by May 2001 and ended by January 2004.

Pre-operative diagnosis depended upon clinical, laboratory, sonographic and percutaneously derived liver biopsy examination. Identification of the TC sign was included in the pre-operative ultrasound scanning.

They all had undergone rigorous ultrasound scanning using both 5 MHz and 7 MHz probes (Toshiba (Tokyo, Japan) apparatus Sonolayer 250 SSA equipped with both 5 MHz and 7 MHz convex liner transducers) done prior to surgery, at 2 weeks, bimonthly for 3 months, monthly for 2 months and then every 3 months post-operatively. Hepatomegaly was considered clinically by assessing liver span and confirmed by ultrasound. The used measurement was the length of the liver on the sagittal view in the mid-clavicular line which usually corresponds to the mid-hepatic line and midline and compared with age related norms [13]. This was aided by detection of indirect signs of hepatomegaly including extension of the right lobe below the lower pole of the right kidney (in the absence of a Riedel's lobe), rounding of the caudal margin of the liver on the sagittal view, and extension of the left lobe into the left upper quadrant above the spleen [14].

Each scan was performed by one of the first three authors and for every examination the scan was done twice by two examiners independent of each other on same day and a decision was considered if both findings were found to be congruent. All authors were blinded to results of previous scans.

The findings were correlated to intraoperative surgical findings, type of procedure and immediate post-operative events. They were also correlated to clinical outcome, occurrence of cholangiopathy, other post-operative complications and liver function tests. The outcome was graded as outcome A (successful biliary drainage), outcome B (improved and sustained moderate bile flow), outcome C (chronic disease) and outcome D (death). Successful biliary drainage was defined as normal bilirubin levels and maintained alanine aminotransferase (ALT) levels within and below double the highest normal level, persistence of coloured stools with or without presence of hepatosplenomegaly and/or portal hypertension. Improved and sustained moderate bile flow was defined as having ALT within and below four times the highest normal level. It included those who had a stable disease albeit with compromised quality of life, or compromised growth. Chronic progressive disease was defined as persistence of cholestasis, where bilirubin level was higher than four times the upper limit of normal. It included those who had a compromised synthetic function and progressive disease with severe hepatocelluar dysfunction. The group having outcome D included those who died from progressive disease within 18 months of operative intervention.


   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 References
 
The 27 infants were studied prospectively. The duration of the study was 33 months; the mean duration of follow-up was 5.9±3.4 months (range 3.5–21 months) with a total of 122 performed ultrasound examinations (mean ultrasound examinations per infant 4.9±1.6). Nine (33.3%) were males and 18 (66.6%) females.

The mean age at portoenterostomy was 72.8±17.7 days.

Clinical picture and evaluation
All showed TC sign upon pre-operative ultrasound evaluation. Percutaneous liver biopsy was confirmatory in all patients. Of the 27 infants only 2 were above 90 days at the time Kasai procedure was performed.

Operative procedure
All children had undergone hepato-portoenterostomy. In depth removal of all fibrous cone and exposure of denuded porta beyond the skeletonized branching portal veins was performed in 9 (33.3%) infants, and superficial shaving of the extrahepatic ducts that were cut free from the portal plate on a level with that of the capsule of liver along with lateral dissection in 8 (29.6%) infants. In depth removal of all fibrous cone with exposure of liver parenchyma to its capsule without dissection of portal vein branches was done in another 9 (33.3%) infants with missing intraoperative details in one infant.

Ultrasound findings
14 infants (53.8%) were found to have a post-operative TC sign. Those with a post-operatively positive TC sign remained positive throughout the study. It did not reappear in an initially post-operatively TC sign negative infant. The post-operative ultrasound showed that 22 (81.5%) were found to have hepatomegaly (above 95th percentile for age related norms), 3 (11.1%) had attenuation of hepatic veins, 3 (11.1%) were found to have thrombosed portal vein (all underwent in depth removal of all fibrous cone without portal vein dissection). 19 (70.4%) were found to have splenomegaly (above 95th percentile for age related norms) and 10 (37.0%) were found to have ascites.

Outcome of children
Of the 27 infants studied prospectively, 3 (11.1%) were jaundice-free post-operatively having successful biliary drainage (outcome A). Seven (25.9%) infants improved and sustained moderate bile flow (outcome B). Nine (33.3%) infants developed chronic progressive disease post-operatively and 7 (25.9%) died within the first 18 months post-operatively. The grave outcome is pronounced as liver transplantation is not yet an established available treatment modality in Cairo University Hospitals. Outcome according to portoenterostomy procedure is illustrated in Table 1Go.


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  		Table 1. Outcome according to surgical procedure

 
Correlations
The infants displaying post-operative TC sign upon ultrasound had undergone superficial shaving and lateral dissection and in depth removal of all fibrous cone without dissection of portal vein branches; none had undergone in depth removal of all fibrous cone with dissection of portal vein branches (Table 2Go).


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  		Table 2. Post-portoenterostomy triangular cord (TC) sign according to surgical procedure

 
They had higher direct bilirubin levels compared with those without (5.5±4.4 versus 2.5±1.8 mg%, p=0.031), splenomegaly (Chi squared p=0.01), were more liable to repeated cholangitis compared with those without (2.4±2 versus 0.8±0.6 episodes for the first 8 months post-operatively, p=0.014) and their outcome was worse in terms of mortality than the others without (Chi squared p=0.045).

An unfavourable outcome was associated with the presence of hepatomegaly (Chi squared p=0.022), ascites (Chi squared p=0.041, Kasai modification (Chi squared p=0.026) and presence of TC sign post-operatively (Chi squared p=0.036). Age at Kasai procedure (under 60 days or above) did not correlate with outcome (Chi squared p=0.326).

Surgical procedure predicted the post-operative TC sign (p=0.001 using linear regression analysis) and the presence of TC sign predicted poor outcome (p=0.001 using linear regression analysis) with 86.6% sensitivity and 72.7% specificity.


   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
References
 
This is the first report evaluating the post-operative ultrasound presence of TC sign. We have previously reported a diagnostic accuracy of 95% with 85% sensitivity and 100% specificity in biliary atresia [5]. The rigorous protocol followed post-operatively showed that it did not recur as it did not reappear in any of the infants who had an absent TC sign in a post-operative ultrasound.

Its presence correlated with the depth of removal of all fibrous cone and exposure of denuded porta beyond the skeletonized branching portal veins at surgical portoenterostomy, where deep removal and exposure were associated with an absent ultrasound TC sign post-operatively. Others have also stressed the importance of dissection at the porta hepatis as a crucial step in surgery for biliary atresia [15].

A negative TC sign was associated with better outcome of the infants with biliary atresia and no deaths.

Outcome of biliary atresia has changed dramatically with the advent of liver transplantation [16]. Innovative surgical techniques, particularly living related donor graft, allowed successful transplantation in infants [17]. Yet interest in Kasai portoenterostomy became underscored as Diem et al have reported that best results in children undergoing transplantation were obtained after 6 years of age [18]. This indicates the importance of performing a Kasai portoenterostomy as the first therapeutic step in biliary atresia.

The short term benefit of hepatoportoenterostomy is decompression and drainage sufficient to forestall the onset of cirrhosis and sustain growth until a successful liver transplantation can be performed [19]. Successful hepatic portoenterostomy depends on early diagnosis and operation, adequate operative technique, surgeon experience, prevention of post-operative cholangitis and precise post-operative management.

The fact that the pathophysiology of the liver and of the intrahepatic bile ducts in this disease is obscure [20] is reflected by the lack of an absolutely precise positive predictive factor with high sensitivity and specificity.

In search of positive predictors of outcome of infants and children, Emblem et al reported that the median survival in infants operated on before the age of 60 days was significantly longer than the survival of children operated on after the age of 60 days, and surgical intervention within the first 2 months of life in infants with extrahepatic biliary atresia was suggested [21].

However, age was not the only prognostic parameter as there were reports of successful hepatoportoenterostomy at age 132 days despite a delay in diagnosis [22, 23]. Changes characteristic of biliary atresia may appear even after 9 weeks of age. Bile duct paucity and normal bile duct to portal space ratio do not preclude the subsequent development of biliary atresia [24]. Racial differences were also studied as potential predictors of or influences on outcome [25].

Regarding the surgical technique of portoenterostomy and presence of post-portoenterostomy TC sign influence outcome, the predictive value of post-portoenterostomy TC sign (86.6% sensitivity and 72.7% specificity) is low, which renders it a guiding tool rather than a prognostic one. Its use with other parameters in a prognostic scoring system needs to be further investigated. The value of post-portoenterostomy TC sign is more of an assessment tool of adequacy of surgical intervention, surgeon experience and operative contribution to outcome. The need for deep removal of fibrous cone and the use of intraoperative TC sign detection by ultrasound to guide the depth of the surgical procedure is underscored.

Finally we report that the presence of TC sign upon ultrasound examination of infants having undergone hepatoportoenterostomy is associated with more morbidity and mortality, and reflect inadequate surgical technique.

Received for publication November 13, 2004. Revision received April 22, 2005. Accepted for publication April 25, 2005.


   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

  1. Lee HJ, Lee SM, Park WH, Choi SO. Objective criteria of triangular cord sign in biliary atresia on US scans. Radiology 2003;229:395–400.[Abstract/Free Full Text]
  2. Park WH, Choi SO, Lee HJ, Kim SP, Zeon SK, Lee SL. A new diagnostic approach to biliary atresia with emphasis on the ultrasonographic triangular cord sign: comparison of ultrasonography, hepatobiliary scintigraphy, and liver needle biopsy in the evaluation of infantile cholestasis. J Pediatr Surg 1997;32:1555–9.[CrossRef][Medline]
  3. Visrutaratna P, Wongsawasdi L, Lerttumnongtum P, Singhavejsakul J, Kattipattanapong V, Ukarapol N. Triangular cord sign and ultrasound features of the gall bladder in infants with biliary atresia. Australas Radiol 2003;47:252–6.[CrossRef][Medline]
  4. Kanegawa K, Akasaka Y, Kitamura E, Nishiyama S, Muraji T, Nishijima E, et al. Sonographic diagnosis of biliary atresia in pediatric patients using the "triangular cord" sign versus gallbladder length and contraction. AJR Am J Roentgenol 2003;181:1387–90.[Abstract/Free Full Text]
  5. Kotb MA, Kotb A, Sheba MF, El Koofy NM, El-Karaksy HM, Abdel-Kahlik MK, et al. Evaluation of the triangular cord sign in the diagnosis of biliary atresia. Pediatrics 2001;108:416–20.[Abstract/Free Full Text]
  6. Pinter AB, Farkas A, Par A, Kovesi T, Appelshoffer S. A long-term follow-up of five patients with atresia of the common bile duct. J Pediatr Surg 2004;39:1050–4.[Medline]
  7. Visser BC, Suh I, Hirose S, Rosenthal P, Lee H, Roberts JP, et al. The influence of portoenterostomy on transplantation for biliary atresia. Liver Transpl 2004;10:1279–86.[Medline]
  8. Grabhorn E, Schulz A, Helmke K, Hinrichs B, Rogiers X, Broering DC, et al. Short- and long-term results of liver transplantation in infants aged less than 6 months. Transplantation 2004;78:235–41.[Medline]
  9. Tannuri U, Velhote MC, Santos MM, Gibelli NE, Ayoub AA, Maksoud-Filho JG, et al. Pediatric liver transplantation: fourteen years of experience at the children institute in São Paulo, Brazil. Transplant Proc 2004;36:941–2.[Medline]
  10. Nio M, Ohi R, Miyano T, Saeki M, Shiraki K, Tanaka K. Japanese Biliary Atresia Registry: Five- and 10-year survival rates after surgery for biliary atresia: a report from the Japanese Biliary Atresia Registry. J Pediatr Surg 2003;38:997–1000.[CrossRef][Medline]
  11. Baerg J, Zuppan C, Klooster M. Biliary atresia—a fifteen-year review of clinical and pathologic factors associated with liver transplantation. J Pediatr Surg 2004;39:800–3.[Medline]
  12. Uchida K, Urata H, Suzuki H, Inoue M, Konishi N, Araki T, et al. Predicting factor of quality of life in long-term jaundice-free survivors after the Kasai operation. J Pediatr Surg 2004;39:1040–4.[Medline]
  13. Abd-El Ghafar S, Bahaa El-Din HK, Seoud I, Salah S. Ultrasonographic measurements of normal liver in early childhood. Thesis submitted in partial fulfillment in Master's degree in Paediatrics, Cairo University, 1992.
  14. Kurtz AB, Middleton WD. Liver. In: Kurtz AB, Middleton WD, editors. Ultrasound: the requisites. St Louis, MO: Mosby–Year Book, 1996:5.
  15. Toyosaka A, Okamoto E, Okasora T, Nose K, Tomimoto Y, Seki Y. Extensive dissection at the porta hepatis for biliary atresia. J Pediatr Surg 1994;29:896–9.[Medline]
  16. Shinkai M, Ohhama Y, Take H, Fukuzato Y, Fujita S, Nishi T. Evaluation of the PELD risk score as a severity index of biliary atresia. J Pediatr Surg 2003;38:1001–4.[Medline]
  17. Alonso EM, Neighbors K, Mattson C, Sweet E, Ruch-Ross H, Berry C, et al. Functional outcomes of pediatric liver transplantation. J Pediatr Gastroenterol Nutr 2003;37:155–60.[CrossRef][Medline]
  18. Diem HV, Evrard V, Vinh HT, Janssen M, Otte JB, Reding R. Pediatric liver transplantation for biliary atresia: results of primary grafts in 328 recipients. Transplantation 2003;75:1692–7.[Medline]
  19. A-Kader HH, Balisteriri WF. Cholestasis. In: Behrman RE, Kleigmen RM, Jenson HB editors. Nelson textbook of pediatrics, 17th edn. Philadelphia, PA: W. B. Saunders Company, 2004:1315–9.
  20. Ohi R. Surgery for biliary atresia. Liver 2001;21:175–82.[Medline]
  21. Emblem R, Stake G, Monclair T. Progress in the treatment of biliary atresia: a plea for surgical intervention within the first two months of life in infants with persistent cholestasis. Acta Paediatr 1993;82:971–4.[Medline]
  22. Bielamowicz A, Weitzman JJ, Alshak NS, Rosenthal P. Successful late Kasai portoenterostomy. J Pediatr Gastroenterol Nutr 1992;14:232–6.[Medline]
  23. Davenport M, Puricelli V, Farrant P, Hadzic N, Mieli-Vergani G, Portmann B, et al. The outcome of the older (> or =100 days) infant with biliary atresia. J Pediatr Surg 2004;39:575–81.[Medline]
  24. Azar G, Beneck D, Lane B, Markowitz J, Daum F, Kahn E. Atypical morphologic presentation of biliary atresia and value of serial liver biopsies. J Pediatr Gastroenterol Nutr 2002;34:212–5.[Medline]
  25. Lee H, Lewis J, Schoen BT, Brand T, Ricketts RR. Kasai portoenterostomy: differences related to race. J Pediatr Surg 2001;36:1196–8.[Medline]




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