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  Table of Contents    
ORIGINAL ARTICLE  
Year : 2014  |  Volume : 57  |  Issue : 3  |  Page : 380-385
A histopathological study of liver and biliary remnants in the long-term survivors (>10 years) of cases of biliary atresia


1 Department of Pathology, Institute of Post Graduate Medical Education and Research, Kolkata, West Bengal, India
2 Department of Pathology, KPC Medical College and Hospital, Jadavpur, Kolkata, West Bengal, India
3 Park Children's Centre for Treatment and Research, Kolkata, West Bengal, India

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Date of Web Publication14-Aug-2014
 

   Abstract 

Context: Biliary atresia (BA) is a destructive process affecting both extra- and intra-hepatic bile ducts leading to fibrosis and obliteration of the biliary tree and cirrhosis usually within 2 years. Factors influencing the outcome of portoenterostomy (PE) have not been clearly defined. Aims: Our aim was to identify children with no evidence of liver disease 10 years or more after PE and to compare the pathology of liver and biliary remnants in this group with those associated with poor outcome. Settings and Design: Prospective observational study. Materials and Methods: Wedge biopsies of liver and portal remnants, taken at the time of PE, where available, were reviewed. The parameters studied were - presence of large bile ducts (>150 μ), degree of fibrosis and bile duct proliferation (BDP), presence of ductal plate malformation (DPM) and age at operation. Statistical Analysis Used: Fisher's exact test with Freeman Halton extension for univariate analysis and Logistic regression analysis as multivariate analysis. Results: Of 68 cases operated between 1995 and 2001, 14 patients survived >10 years and 54 were associated with poor outcome. Large ducts were significantly more in survivors (70% vs. 26%, P = 0.02). DPM was not seen in any of the survivors and was present in 24% of poor outcome group. Fibrosis and BDP were also significantly less among the survivors (P < 0.001, P = 0.03, respectively). The mean ages at operation in the two groups were 66.8 and 89.6 days, respectively. Conclusion: From this study, we feel that lower degree of fibrosis and BDP, absence of DPM, presence of large ducts and younger age at operation were associated with better long-term outcome. Of these, degree of fibrosis was the most significant factor.

Keywords: Bile duct proliferation, ductal plate malformation, extra-hepatic biliary atresia, long-term prognosis Key Messages: Long Term Histological prognostic factors are not clearly defined for Extrahepatic Biliary Atresia. Aiming to identify those in our study, we emphasize that, lower degree of fibrosis and ductular proliferation, absence of ductal plate malformation and wider ducts at surgery were associated with better long term(<10 years) outcome

How to cite this article:
Mukhopadhyay SG, Roy P, Chatterjee U, Datta C, Banerjee M, Banerjee S, Basu AK, Ganguli M. A histopathological study of liver and biliary remnants in the long-term survivors (>10 years) of cases of biliary atresia. Indian J Pathol Microbiol 2014;57:380-5

How to cite this URL:
Mukhopadhyay SG, Roy P, Chatterjee U, Datta C, Banerjee M, Banerjee S, Basu AK, Ganguli M. A histopathological study of liver and biliary remnants in the long-term survivors (>10 years) of cases of biliary atresia. Indian J Pathol Microbiol [serial online] 2014 [cited 2021 Apr 13];57:380-5. Available from: https://www.ijpmonline.org/text.asp?2014/57/3/380/138722



   Introduction Top


Biliary atresia (BA) is a devastating disease of infants which, if untreated, invariably leads to liver failure, cirrhosis, and death. It is the most common indication for pediatric liver transplantation (LT) throughout the developed world. Biliary atresia is defined as a complete fibrous obliteration of a portion or of entire extra-hepatic biliary tree not associated with calculi, neoplasm, or trauma. [1] It is an inflammatory fibrosing process involving both the extra- and intra-hepatic biliary tree resulting in fibrous obliteration of the biliary tract. The etiology is largely unknown. However, extra-hepatic biliary atresia (EHBA) is a phenotypic expression of diverse insults received either during intrauterine life or in the perinatal period.

In 1959, Kasai and Suzuki introduced hepatic portoenterostomy (PE) to reestablish bile flow in BA. [2] Sequential treatment by Kasai operation and LT if needed is currently recommended for BA. [3] In our setting where availability and affordability of LT is limited, Kasai operation may be the only chance of survival for BA patients. Although, extended survival has been reported from many centers factors affecting outcome have not been defined clearly.

To understand the role of Kasai operation in BA it is important to analyze the outcome and the present status of survivors who have retained their native liver after successful procedure. There are many studies assessing the short-term prognosis of Kasai portoenterostomy (KPE), but there is little data available on its outcome into late childhood or early adulthood. [4],[5],[6]

Age at operation and extent of fibrosis at KPE have been considered as critical factors in determining postoperative prognosis, and higher age has been consistently linked with a worse prognosis. [7],[8],[9],[10],[11],[12] The other prognostic factors are the presence of ductal plate malformation, extent of cholestasis, bile duct proliferation (BDP) and presence of large sized bile ducts at porta. However, results so far are inconclusive. This study aims to retrospectively identify children with no evidence of liver disease 10 years or more after KPE and to compare the pathology of liver and biliary remnants in this group with those associated with poor outcome.


   Materials and methods Top


Data from infants who were operated for KPE for BA in our center from 1995 to 2001 were taken. Details of those who had no surgical complications, normal bilirubin, normal aspartate aminotransferase (AST), alkaline phosphatase (ALP), normal serum albumin, normal international normalized ratio, and platelet count were noted. BULIDA (Tc-99m-mebrofenin) scan was done on all cases as a part of preoperative preparation. Follow-up was done in all cases by ultrasonography whole abdomen and liver function test (LFT) every 6 months. Surgical complications included signs of portal hypertension, liver enlargement, increased firmness of liver, episodes of cholangitis and increase in clinical jaundice. Failure, henceforth termed as poor outcome, was determined by death, transplant or ongoing liver failure after 10 years postprocedure.

Diagnosis of EHBA was confirmed by histological examination of liver and biliary remnants after KPE and by intra-operative cholangiography in most cases. The wedge biopsies of liver and portal remnants, wherever available, were sent for histopathological examination and were stained with hematoxylin and eosin and Masson's trichrome stain. The parameters assessed were: Age at operation, presence of large bile ducts (>150 μ), degree of fibrosis, BDP and presence of ductal plate malformation. The extent of fibrosis was evaluated according to the fibrosis score described by Weerasooriya et al. [13] Mild (grade I) ranged from portal fibrous expansion to porto-portal bridging fibrosis involving <50% of portal tracts; moderate (grade II) included cases with similar bridging fibrosis involving >50% of portal tracts without nodular architecture; and severe (grade III) comprised cases with porto-portal and porto-central bridging fibrosis involving >50% of portal tracts, accompanied by nodular architecture. Bile ductal proliferation was considered to be present if the average number of ducts in the portal tract was >5. A semi-quantitative scoring system [14] was used to grade the degree of BDP: Mild, average number of bile ducts per portal tract between 5 and 9; moderate, average number of bile ducts per portal tract ≥10; severe, elongated attenuated angulated bile ducts in addition to proliferation (average number of bile ducts per portal tract ≥10).

Ductal plate malformation was recognized by the presence of unusual curved or concentric pattern sometimes found around a fibrous or vascular core within the portal tracts and IHC for pancytokeratin was done to recognize this unusual pattern and also to grade the degree of BDP. [4] Immunostaining for pancytokeratin (Biogenex, USA) was done using standard immunohistochemical protocol. Bile duct morphometry was done using an ocular morphometer (ERBA, Japan) which was calibrated using an improved Neubauer's chamber. Presence and number of large bile ducts (>150 μ) or complete absence of ducts was noted. Four cases of age matched controls were used. All slides were reviewed by two pathologists and difference of opinion was solved by common consensus. Statistical analysis was carried out using computer software Statistica version 6 (StatSoft Inc., Tulsa, Oklahoma, USA, 2001).


   Results Top


Of 68 cases operated between 1995 and 2001, 42 (71.43%) were boys and 26 (28.57%) were girls, respectively. Fourteen (20.58%) patients survived more than 10 years with no evidence of liver disease and the rest were associated with poor outcome. All cases underwent KPE following no excretion of dye even after 24 h. LFT of the survivors at the time of surgery ranged from mean serum bilirubin (16.71 ± 4.286 mg/dl), mean ALP (1224.07 ± 395.305 U/L), mean AST (430.93 ± 171.793 IU/L), and mean gamma glutamyl transpeptidase (GGT) (612.43 ± 235.122 IU/L). At 6 months postoperatively, the LFT of the survivors showed the following - mean serum bilirubin (1.94 ± 0.745 mg/dl), mean ALP (364.50 ± 191.598 U/L), mean AST (82.50 ± 47.591 IU/L), and mean GGT (76.57 ± 54.194 IU/L) 6 months postprocedure, respectively. The survivors have normal LFT after 10 years of follow-up and up to the present time, but the serum bilirubin hovered around 1.5-2.2 mg/dl. A single episode of cholangitis was noted in 12% of the survivors, postprocedure within the first 2 years. Two of them (among 14) had multiple episodes of cholangitis, whereas in the poor outcome group, 44% presented with at least one episode of cholangitis in the early postoperative period.

The average age of operation among the survivors was 66.8 days. It was 89.6 days for the poor outcome group. Although this difference was not found to be significant, we noted a trend toward a worse prognosis with increasing age [Table 1].
Table 1: Age at operation, large bile ducts and DPM in survivors and poor outcome group

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Of the 68 patients bile duct morphometry could be done in only 49. In many cases, the portal plaque is flimsy or covers a very small area and cannot be excised properly for histopathological studies and measurements. Hence, only the cases in which a reasonable sample of tissue from the portal area for histopathological studies could be harvested were evaluated and presented. The other cases nevertheless had BA as per histopathological examination of the liver, but the measurements were not possible in these cases. Of the 49, 10 patients were survived, and 39 were associated with poor outcome. Large bile ducts (>150 μ) were found in seven cases among the survivors (70%) compared to only 26% of the poor outcome group. Three (30%) patients who are alive had bile duct diameter at surgery of <150 μ compared to 29 (74%) patients of the poor outcome group. This data were found to be statistically significant (P value 0.021) [Table 1], [Figure 1]a-c.
Figure 1: Photomicrographs of tissue taken from portal plaque. (a) Low power view showing duct >150 ƒÝ, (b) High power view of the above showing desquamati on of epithelium and inflammation (H and E stain), and (c and d) Portal plaque, solid type lacking in biliary channels, high and low power view

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The degree of fibrosis was categorized as mild, moderate, and severe. Among the 68 patients mild, moderate, and severe fibroses were found in 13, 28, and 27 patients, respectively. Among the 14 survivors 8 (57%) showed mild fibrosis, 5 (36%) had moderate fibrosis, and there was a single case of severe fibrosis. In the poor outcome group, 5 (9%), 26 (48%), and 23 (43%) patients showed mild, moderate, and severe fibrosis, respectively. A highly significant correlation was noted between severity of fibrosis and poor outcome (P < 0.001) [Table 2], [Figure 2]a-c.
Table 2: Degree of fibrosis among the survivors and poor outcome group

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Figure 2: Photomicrographs showing different degrees of fibrosis: (a) Mild, (b) Moderate, (c and d) Severe (H and E stain)

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Among the 68 cases assessed 7, 35, and 26 patients had mild, moderate, and severe BDP, respectively. Among the survivors, 4 (29%), patients had mild, 7 (50%) moderate, and 3 (21%) had severe degree of BDP compared to 3 (5%), 28 (52%), and 23 (43%) patients of poor outcome group, respectively. This data were also significant statistically (P value 0.035) [Table 3], [Figure 3] and [Figure 4] a-c.
Table 3: Grade of BDP among the survivors and poor outcome group

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Figure 3: Photomicrographs showing varying grades of bile ductular proliferation: (a) Mild, (b) Moderate, (c and d) Severe in low and high power respectively (H and E stain)

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Figure 4: Immunostaining for cytokeratin antibody for showing the degree of bile duct proliferation. (a) Low power view and (b) High power view of severe degree of ductular proliferation with prominent fibrosis

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Ductal plate malformation as a whole was present in 13 (19%) patients. DPM was not seen in any of the survivors, but was present in 24% of the 54 patients of poor outcome [Figure 1]a-c group (P value 0.055). This data were also significant [Table 1], [Figure 5]a-c.
Figure 5: Photomicrographs of sections of liver taken from cases of ductal plate malformation. (a) Irregular clusters of misshapen and curvilinear bile ducts arranged around small arterioles. (b) High power view showing misshapen ducts with overgrowth of underlying connective tissue (H and E stains)

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Multivariate analysis using binary logistics regression analysis was attempted taking the age at operation, degree of fibrosis, portal morphometry, and BDP into account. The outcome of these individual factors was not statistically significant in this logistics regression analysis (Nagelkerke R Square 0.500). However, there was a positive association between survival and lower degree of fibrosis. Association was also noted between large bile ducts, lower BDP and survival. This multivariate analysis showed the strongest association of survival with a degree of fibrosis followed by portal morphometry and BDP. No such trend was observed between age at operation and survival.


   Discussion Top


Since decades KPE has become the standard surgical procedure for BA worldwide. The outcome after KPE is thought to be to be influenced by various factors such as the type of anatomical abnormality, age at initial operation, experience of the surgical center, era in which surgery was performed and postoperative medical care. Long-term survival after KPE still remains uncommon and there are no uniform criteria (histopathological or other) for defining long-term success. Global survival rates of BA patients >10 years following KPE ranges from 15% to 53%. [15],[16],[17],[18],[19],[20],[21],[22] In a nationwide survey of major pediatric centers in Japan, only 325 of 2013 (16.1%) patients survived for more than 10 years after KPE and only 157 (7.8%) remained jaundice-free with normal liver function. [25] In our study of 68 patients, 14 survived (21%) more than 10 years.

Interpretation of liver histology for the prognosis of BA, in the long-term, is a difficult due to lack of sizable cohort. Until now, many histopathological prognostic factors have been implicated. The risk of failure after PE for biliary atresia is related to age at operation and the anatomy and histology of the atretic extra-hepatic bile ducts. [19] Rastogi et al. [27] and Santos et al. [28] have identified portal ductal proliferation, bile plugs in the ductules and portal fibrosis as important indicators of BA. Ohya et al. have observed that survival 10 years after PE was associated with the resolution of jaundice in the postoperative period, age at surgery, extent of fibrosis, and size of bile ducts in the porta hepatis. [46 It must also be considered that the histopathology of liver in biliary atresia is a dynamic and age dependent process. [29]

Wide portal ductules at operation ensure proper bile flow following surgery. Failure to establish biliary flow after Kasai procedure as evidenced by continuing acholic stools is associated with future need for transplantation. To consider PE successful many investigators recommend that portal plate ductules measure a minimum of 150 μ. [19],[30] Baerg et al. have shown that the average size of portal ductules of patients who never required transplantation 15 years following Kasai procedure was 247 μ. Nearly, all patients who had bile duct diameter of <100 μ needed a transplantation and this association was statistically significant. [31] Altman et al. while analyzing multivariate risk factor analysis in 126 patients over 25 years has shown that ductal histology as a highly significant independent risk factor and ductal diameter >150 μ was associated with the best prognosis. [19] Schweizer et al. have also confirmed that morphologic pattern of the porta hepatis at surgery is an important prognostic indicator. [32] Chandra et al. as well as Raweily et al. and Tan et al. have also shown that smaller sized ductules correlate with a worse prognosis. [33],[34],[ - 7] However, their studies were conducted over relatively shorter period of time. Studies carried over a longer period of time (15 years or more) have also shown similar results. [35 ] Wildhaber et al. have shown in a study spanning nearly 3 decades on 81 postoperative patients of KPE that cirrhosis (bridging fibrosis) in the liver biopsy, duct size <150 μ diameter at the time of PE, and the number of cholangitic episodes postoperatively were negative risk factors for a successful outcome. [36] Gautier et al. have demonstrated that bile duct profiles of 150 μ or greater, particularly if lined with columnar epithelium, have been associated with a good surgical result. [37]

The intrahepatic bile ducts (IHBD) develop from the fetal ductal plate through an orderly process of selection and deletion called ductal plate remodeling. Disturbances in this process are believed to give rise to DPM, in which parts of the IHBD retain the fetal configuration. The occurrence of DPM has been reported consistently in a section of patients of biliary atresia; however, the incidence of occurrence ranges from 14% to 50%, respectively. [4],[27],[34],[39],[40],[],[41] The range of the percentage is rather wide. This could be due to ethnic and geographic differences and also due to the fact that diagnostic criteria of DPM are not clearly defined. The prognostic importance of presence of DPM in liver biopsy in EHBA has first reported by Low et al. and they have found the incidence of DPM in BA to be 38%. [ 38] Awasthi et al. have reported the incidence of DPM in cases of BA to be 26%. [40] Shimadera et al. in a recent study reported that the presence of DPM in the liver predicts poor bile flow after hepatoportoenterostomy in infants with BA. [42] In our own series published earlier the incidence was found to be 15%, [4] and in the present series, it was 19% (13/68) overall and 24% (13/54) of the poor outcome group who were associated with poor prognosis.

Biliary fibrosis at operation is an independent prognostic factor for BA. [36],[41] In a landmark study on 47 postoperative BA patients Santos et al. have demonstrated that biliary fibrosis and bile ductular proliferation are directly related and as fibrosis score increased BDP also increased proportionately. They have also demonstrated an inverse relationship of this association with prognosis of BA patients. [28] Tan et al. [7] confirmed these views in their independent study. Shteyer et al. demonstrated the relationship between the fibrosis score and smooth muscle actin expression in the long-term survivors of KPE. [44] In our study, we found that fibrosis at surgery to be the most significant predictor of long-term outcome. Bittmann et al. in a single institution study reported that the presence of cirrhosis portends a poorer prognosis and may be an indication for early transplantation. [47] Wildhaber et al. in their study spanning 27 years have shown that bridging hepatic fibrosis at KPE is an independent negative predictive factor. [36]

Bile ductular proliferation, is one of the most important diagnostic marker for EHBA [48] and is a constant finding in biliary atresia except the very early stages. [45] However, its prognostic utility was first reported by Santos et al. (2009). They reported that the extent of biliary proliferation at PE, was associated with survival of BA patients. [28] There are only a few studies available on prognostic implication of BDP in EHBA. In our study, we also found BDP to be of prognostic utility for long-term survival.

Age at Kasai operation is a critical factor not only in determining the long-term success, but also on the presence of degree fibrosis on initial biopsy, gross pattern, and histological findings of biliary remnants. In their study, Altman et al. [19] have shown that there was no increased risk of failure comparing the outcomes between the intermediate group (50-70 days) with those operated before 49 days. However, older patients (71 days or more) were at significantly higher risk of failure when compared to either of the patient cohorts (P = 0.0077). Sanghai et al. [6] in their series of 37 patients concluded that PE before 3 months of age has a better outcome. While reviewing different study series, Goanta et al. in their meta-analysis found that age <10 weeks at operation, preoperative histology and ductal remnant size could predict improved long-term outcome at KPE. [23] Hung et al. noted a change in the pattern of survival with the age at which Kasai operation is performed and the survival disadvantage of infants operated after 120 days [16] . Shinkai et al. [24] have reported age at the time of Kasai operation (<70 days vs. >70 days) resulted in a significant difference in 20 years survival rate. However, in a recent study, Davenport et al. have shown that potential for reasonable medium-term survival is present in about one-third of infants who underwent primary corrective surgery at 100 days or more. [26] In our long-term study also, age did not prove to be an important predictive factor in both uni- and multi-variate analyses.


   Conclusion Top


From this study, we feel that lower degree of fibrosis, presence of large ducts, lower degree of BDP and absence DPM were associated with a better outcome. Of these, degree of fibrosis was the most significant factor in univariate as well as multivariate analysis.


   Acknowledgment Top


We are grateful to Prof. S.K. Chatterjee for sharing his cases with us. We are alo grateful to Prof. Avijit Hazra for statistical analysis.

 
   References Top

1.
Kahn E. Biliary atresia revisited. Pediatr Dev Pathol 2004;7:109-24.  Back to cited text no. 1
    
2.
Kasai M, Suzuki H, Ohashi E, Ohi R, Chiba T, Okamoto A. Technique and results of operative management of biliary atresia. World J Surg. 1978;2:571-579.  Back to cited text no. 2
    
3.
Otte JB, de Ville de Goyet J, Reding R, Hausleithner V, Sokal E, Chardot C, et al. Sequential treatment of biliary atresia with Kasai portoenterostomy and liver transplantation: A review. Hepatology 1994;20:41S-8.  Back to cited text no. 3
    
4.
Roy P, Chatterjee U, Ganguli M, Banerjee S, Chatterjee SK, Basu AK. A histopathological study of liver and biliary remnants with clinical outcome in cases of extrahepatic biliary atresia. Indian J Pathol Microbiol 2010;53:101-5.  Back to cited text no. 4
[PUBMED]  Medknow Journal  
5.
Sookpotarom P, Vejchapipat P, Chittmittrapap S, Sookpotarom P, Vejchapipat P, Chittmittrapap S, et al. Short-term results of Kasai operation for biliary atresia: Experience from one institution. Asian J Surg 2006;29:188-92.  Back to cited text no. 5
    
6.
Sanghai SR, Shah I, Bhatnagar S, Murthy A. Incidence and prognostic factors associated with biliary atresia in western India. Ann Hepatol 2009;8:120-2.  Back to cited text no. 6
    
7.
Tan CE, Davenport M, Driver M, Howard ER. Does the morphology of the extrahepatic biliary remnants in biliary atresia influence survival? A review of 205 cases. J Pediatr Surg 1994;29:1459-64.  Back to cited text no. 7
    
8.
Langenburg SE, Poulik J, Goretsky M, Klein AA, Klein MD. Bile duct size does not predict success of portoenterostomy for biliary atresia. J Pediatr Surg 2000;35:1006-7.  Back to cited text no. 8
    
9.
McKiernan PJ, Baker AJ, Kelly DA. The frequency and outcome of biliary atresia in the UK and Ireland. Lancet 2000;355:25-9.  Back to cited text no. 9
    
10.
Perlmutter DH, Shepherd RW. Extra hepatic biliary atresia: A disease or a phenotyepe? Hepatology 2002;35:1297-304.  Back to cited text no. 10
    
11.
Laurent J, Gauthier F, Bernard O, Hadchouel M, Odièvre M, Valayer J, et al. Long-term outcome after surgery for biliary atresia. Study of 40 patients surviving for more than 10 years. Gastroenterology 1990;99:1793-7.  Back to cited text no. 11
    
12.
Davenport M. Biliary atresia. Semin Pediatr Surg 2005;14:42-8.  Back to cited text no. 12
    
13.
Weerasooriya VS, White FV, Shepherd RW. Hepatic fibrosis and survival in biliary atresia. J Pediatr 2004;144:123-5.  Back to cited text no. 13
    
14.
Lee WS, Looi LM. Usefulness of a scoring system in the interpretation of histology in neonatal cholestasis. World J Gastroenterol 2009;15:5326-33.  Back to cited text no. 14
    
15.
Nio M, Ohi R, Miyano T, Saeki M, Shiraki K, Tanaka K, et al. 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.  Back to cited text no. 15
    
16.
Hung PY, Chen CC, Chen WJ, Lai HS, Hsu WM, Lee PH, et al. Long-term prognosis of patients with biliary atresia: A 25 year summary. J Pediatr Gastroenterol Nutr 2006;42:190-5.  Back to cited text no. 16
    
17.
Kelly DA, Davenport M. Current management of biliary atresia. Arch Dis Child 2007;92:1132-5.  Back to cited text no. 17
    
18.
Davenport M. Biliary atresia: Outcome and management. Indian J Pediatr 2006;73:825-8.  Back to cited text no. 18
    
19.
Altman RP, Lilly JR, Greenfeld J, Weinberg A, van Leeuwen K, Flanigan L. A multivariable risk factor analysis of the portoenterostomy (Kasai) procedure for biliary atresia: Twenty-five years of experience from two centers. Ann Surg 1997;226:348-53.  Back to cited text no. 19
    
20.
Hadzic N, Davenport M, Tizzard S, Singer J, Howard ER, Mieli-Vergani G. Long-term survival following Kasai portoenterostomy: Is chronic liver disease inevitable? J Pediatr Gastroenterol Nutr 2003;37:430-3.  Back to cited text no. 20
    
21.
Chardot C, Carton M, Spire-Bendelac N, Le Pommelet C, Golmard JL, Auvert B. Prognosis of biliary atresia in the era of liver transplantation: French national study from 1986 to 1996. Hepatology 1999;30:606-11.  Back to cited text no. 21
    
22.
Davenport M, Kerkar N, Mieli-Vergani G, Mowat AP, Howard ER. Biliary atresia: The King's College Hospital experience (1974-1995) J Pediatr Surg 1997;32:479-85.  Back to cited text no. 22
    
23.
Goanta RA, Matusz P, Trestianu V, Popoiu CM. BILIARY ATRESIA Jurnalul Pediatrului 2006;9:33-4.  Back to cited text no. 23
    
24.
Shinkai M, Ohhama Y, Take H, Kitagawa N, Kudo H, Mochizuki K, et al. Long-term outcome of children with biliary atresia who were not transplanted after the Kasai operation: >20-year experience at a children's hospital. J Pediatr Gastroenterol Nutr 2009;48:443-50.  Back to cited text no. 24
    
25.
Miyano T, Fujimoto T, Ohya T, Shimomura H. Current concept of the treatment of biliary atresia. World J Surg 1993;17:332-6.  Back to cited text no. 25
    
26.
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.  Back to cited text no. 26
    
27.
Rastogi A, Krishnani N, Yachha SK, Khanna V, Poddar U, Lal R. Histopathological features and accuracy for diagnosing biliary atresia by prelaparotomy liver biopsy in developing countries. J Gastroenterol Hepatol 2009;24:97-102.  Back to cited text no. 27
    
28.
Santos JL, Kieling CO, Meurer L, Vieira S, Ferreira CT, Lorentz A, et al. The extent of biliary proliferation in liver biopsies from patients with biliary atresia at portoenterostomy is associated with the postoperative prognosis. J Pediatr Surg 2009;44:695-701.  Back to cited text no. 28
    
29.
Dahms B. Liver biopsy interpretation for the 1990's: Clinicopathologic correlations in liver disease. Hepatology 1991;14:S6-8.  Back to cited text no. 29
    
30.
López Gutiérrez JC, Vázquez J, Ros Z, Díaz MC, Larrauri J, Hierro L, et al. Article in Spanish histopathology of biliary atresia: Correlation with biliary flow. Cir Pediatr 1991;4:16-8.  Back to cited text no. 30
    
31.
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.  Back to cited text no. 31
    
32.
Schweizer P, Schweizer M, Schellinger K, Kirschner HJ, Schittenhelm C. Prognosis of extrahepatic bile-duct atresia after hepatoportoenterostomy. Pediatr Surg Int 2000;16:351-5.  Back to cited text no. 32
    
33.
Chandra RS, Altman RP. Ductal remnants in extrahepatic biliary atresia: A histopathologic study with clinical correlation. J Pediatr 1978;93:196-200.  Back to cited text no. 33
    
34.
Raweily EA, Gibson AA, Burt AD. Abnormalities of intrahepatic bile ducts in extrahepatic biliary atresia. Histopathology 1990;17:521-7.  Back to cited text no. 34
    
35.
Maksoud JG, Fauza DO, Silva MM, Porta G, Miura I, Zerbini CN. Management of biliary atresia in the liver transplantation era: A 15-year, single-center experience. J Pediatr Surg 1998;33:115-8.  Back to cited text no. 35
    
36.
Wildhaber BE, Coran AG, Drongowski RA, Hirschl RB, Geiger JD, Lelli JL, et al. The Kasai portoenterostomy for biliary atresia: A review of a 27-year experience with 81 patients. J Pediatr Surg 2003;38:1480-5.  Back to cited text no. 36
    
37.
Gautier M, Elliot N. Extrahepatic hiliary atresia. Morphological study of 98 biliary remnants. Arch Pathol Lab Med 1981;105:397-402.  Back to cited text no. 37
    
38.
Low Y, Vijayan V, Tan CE. The prognostic value of ductal plate malformation and other histologic parameters in biliary atresia: An immunohistochemical study. J Pediatr 2001;139:320-2.  Back to cited text no. 38
    
39.
Terraciano L, Cathomas G, Vecchione R, Tomillo L, Gudat F, Bianchi L. Extra hepatic bile duct atresia associated with hyperplasia of the intrahepatic bile ducts ("early severe" form): High incidence in a South-Italian population. Pathol Res Pract 1995;191:192.  Back to cited text no. 39
    
40.
Awasthi A, Das A, Srinivasan R, Joshi K. Morphological and immunohistochemical analysis of ductal plate malformation: Correlation with fetal liver. Histopathology 2004;45:260-7.  Back to cited text no. 40
    
41.
Arii R, Koga H, Arakawa A, Miyahara K, Lane GJ, Okazaki T, et al. How valuable is ductal plate malformation as a predictor of clinical course in postoperative biliary atresia patients? Pediatr Surg Int 2011;27:275-7.  Back to cited text no. 41
    
42.
Shimadera S, Iwai N, Deguchi E, Kimura O, Ono S, Fumino S, et al. Significance of ductal plate malformation in the postoperative clinical course of biliary atresia. J Pediatr Surg 2008;43:304-7.  Back to cited text no. 42
    
43.
Karrer FM, Lilly JR, Stewart BA, Hall RJ. Biliary atresia registry, 1976 to 1989. J Pediatr Surg 1990;25:1076-80.  Back to cited text no. 43
    
44.
Shteyer E, Ramm GA, Xu C, White FV, Shepherd RW. Outcome after portoenterostomy in biliary atresia: Pivotal role of degree of liver fibrosis and intensity of stellate cell activation. J Pediatr Gastroenterol Nutr 2006;42:93-9.  Back to cited text no. 44
    
45.
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.  Back to cited text no. 45
    
46.
Santos JL, Almeida H, Cerski CT, Silveira TR. Histopathological diagnosis of intra- and extrahepatic neonatal cholestasis. Braz J Med Biol Res 1998;31:911-9.  Back to cited text no. 46
    
47.
Bittmann S. Surgical experience in children with biliary atresia treated with portoenterostomy. Curr Surg 2005;62:439-43.  Back to cited text no. 47
    
48.
Ohya T, Miyano T, Kimura K. Indication for portoenterostomy based on 103 patients with Suruga II modification. J Pediatr Surg 1990;25:801-4.  Back to cited text no. 48
    

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Uttara Chatterjee
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DOI: 10.4103/0377-4929.138722

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