Biliary Complications After Pediatric Liver Transplantation F. Karakayalı, M. Kırnap, A. Akdur, N. Tutar, F. Boyvat, G. Moray, and M. Haberal ABSTRACT Objectives. After liver transplantation, biliary complications are more prevalent in pediatric patients, with reported rates varying between 15% and 30%. Methods. We retrospectively analyzed biliary complications observed in 84 pediatric liver transplantation patients between July 2006 and September 2012. Biliary reconstruction was accomplished via a duct-to-duct anastomosis in 5 (83.3%) of the 6 patients receiving whole liver grafts and in 44 (56.4%) of the 78 patients who received a segmental live donor graft. For the remaining 34 patients with living donor and 1 patient with whole liver graft, Rouxen-Y hepaticojejunostomy was the preferred method. Results. Post-transplantation biliary complications were encountered in 26 patients (30.1%). The biliary complication rate was 38% in 49 duct-to-duct anastomosis, whereas it was 20% in the hepaticojejunostomy group consisting of 35 recipients. Thirteen of the 18 biliary leaks were from duct-to-duct anastomoses and the remaining 5 were from the hepaticojejunostomies and 6 of the 8 biliary strictures were observed in recipients with duct-to-duct anastomosis. In 19 of the 26 patients, the biliary complications were successfully treated with interventional radiologic procedures and 1 was treated with stent placement during endoscopic retrograde cholangiopancreatography. Conclusions. Percutaneous interventional procedures are valuable, effective, and lifesaving therapeutic alternatives for the treatment of bile leaks and strictures after pediatric liver transplantations.
IVER transplantation is an established therapy for children with end-stage chronic liver disease or acute liver failure. However, despite reﬁnements of surgical techniques for liver transplantation in recent years, the incidence of biliary tract complications has remained high and it is still a major challenge for the pediatric liver transplantation (PLT) teams during the surgical procedure and thereafter. In the literature, the incidence of biliary complications in PLT has been reported to occur in 12% to 50% and high rates were observed especially in recipients weighing less than 10 kg.1 The most common complications are bile leaks and biliary strictures, which are the frequent causes of post-transplantation morbidity, graft loss, and death.2 It is well known that biliary complications in PLT are closely associated with the surgical technique and the presence of hepatic artery thrombosis.3 In PLT, especially in living-donor liver transplantation (LDLT), Roux-en-Y hepaticojejunostomy (HJ) is generally accepted as the gold standard technique for biliary reconstruction.4 However, limited numbers of duct-to-duct 0041-1345/13/$esee front matter http://dx.doi.org/10.1016/j.transproceed.2013.09.012 3524
biliary reconstructions have been presented in the literature for pediatric recipients.5e7 Treatment modalities have also changed over the past years toward a primarily nonoperative, endoscopy-based strategy, leaving the surgical intervention for lesions, which otherwise are not curable.3 Although endoscopic treatment is rarely possible in pediatric patients, the majority of these biliary complications can be managed by interventional radiological interventions.8 In this study, our aim is to evaluate the biliary tract complications and their management modalities after PLT in our center.
From the Department of General Surgery (F.K., M.K., A.A., G.M., M.H.) and the Department of Radiology (N.T., F.B.), Baskent University Faculty of Medicine, Ankara, Turkey. Address reprint requests to Feza Karakayali, MD, Department of General Surgery, Baskent University, Fevzi Cakmak Cad. 5. Sok. No:48, Bahcelievler, Ankara 06490, Turkey. E-mail: [email protected]
Crown Copyright ª 2013 Published by Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710 Transplantation Proceedings, 45, 3524e3527 (2013)
Table 1. Demographic Data Compared Regarding Donor Type Characteristics
Deceased Donor (n ¼ 6)
Living Donor (n ¼ 78)
Gender F/M 3/3 25/53 Age (y; mean, range) 8 3 (4e11) 7 (1e17) Weight (kg; mean, range) 24.5 10 (14.5e35) 22 12 (10e32) Child Score (mean, range) 8 2 (6e10) 8 2 (6e10) PELD Score (mean, range) 17 4 (13e21) 18 6 (12e24) Etiology (n) Wilson disease 4 14 Biliary atresia d 8 Cryptogenic 1 15 Fulminant hepatitis d 7 Autoimmune d 7 Hepatitis d 5 Tyrosinemia d 8 Progressive familial 1 12 intrahepatic cholestasis Neonatal cholestasis d 2 Others Operation time (h; mean, 7 1 (6e8) 8 1.5 (6.5e9.5) range) Blood transfusion (U; mean, 1 1 (0e2) 1 1 (0e2) range) Biliary tract reconstruction Hepaticojejunostomy 1 34 Duct-to-duct 5 44 Cold ischemia time 6 2 (4e10) d (h; mean, range)
METHODS From July 2006 to September 2012, 84 PLTs were performed in our center. We retrospectively evaluated the organ source, patients’ age and weight, etiology of end-stage liver disease, type of biliary anastomosis, biliary reconstruction technique, biliary complications, and treatments. All living donors were examined according to our previously reported algorithm for LRLD evaluation.9 Routine intraoperative cholangiography was performed in all donor hepatectomy operations. Duct-to-duct biliary reconstructions were the preferred method for most of the cases; however, in cases with prior portoenterostomy or in reoperations for a biliary leakage, HJs were performed. No trans-anastomotic external biliary drainage catheter was used in these cases. We accepted anastomotic leakages and stenoses as biliary complications, whereas the cut surface leaks and minor ones that were sealed spontaneously without treatment were excluded. Patients with clinical symptoms or biochemical abnormalities demonstrative of biliary complications were evaluated by radiological procedures. All of the patients had ABO blood compatibility with the donor, and they were treated with similar calcineurin inhibitorebased immunosuppression protocols including steroid and mycophenolate mofetil, during the post-transplantation period. The data were analyzed by standard statistical methods and the results were expressed as means SD. Differences between percentages were analyzed using the chi-square test. Probability values of less than .05 were considered signiﬁcant.
Demographic data are given in Table 1 according to graft type. The most common indications for liver transplantation
Table 2. The Biliary Reconstruction Technique in Each Graft Type Duct-to-duct
Right lobe (n ¼ 2) Left lobe (n ¼ 36) Left lateral segment (n ¼ 40) Whole liver (n ¼ 6) Multiple ducts (n ¼ 14)
Deceased Donor (n ¼ 5)
Living Donor (n ¼ 44)
Deceased Donor (n ¼ 1)
Living Donor (n ¼ 34)
d d d
2 20 22
d d d
d 16 18
were Wilson’s disease and cryptogenic cirrhosis. Six patients (7.1%) received a whole liver deceased donor graft whereas the remaining 78 (92.9%) were live donor segmental liver grafts as a result of the low donation rates in our country. All donors were genetically related to the recipient and the majority of them were the parents. In LDLT recipients, 40 (51.3%) received left-lateral segment, 36 (46.2%) received left lobe, and 2 (2.6%) received right lobe grafts. The decision was based on the graft to body weight ratio which has to be more than 1%. Biliary reconstruction was accomplished via a duct-to-duct anastomosis in ﬁve (83.3%) of six patients receiving whole liver grafts and in 44 (56.4%) of 78 patients who received a segmental live donor graft. For the remaining 34 patients with living donor and one patient with whole liver graft, Roux-en Y HJ was the preferred method. Multiple bile ducts were observed in 14 living donor grafts (Table 2). Post-transplantation biliary complications were encountered in 26 patients (30.1%). The biliary complication rate was 38% in 49 duct-to-duct anastomosis, whereas it was 20% in the HJ group consisting of 35 recipients. Thirteen of 18 biliary leaks were from duct-to-duct anastomosis. The remaining ﬁve were from the HJs. Six of eight biliary strictures were observed in recipients with duct-to-duct anastomosis (Table 3). In 8 of 14 grafts with multiple ducts, we preferred to make a duct-to-duct biliary reconstruction. In our series, the rate of biliary complication was 14.3% (2/14) with the existence of multiple ducts. There were nine hepatic arterial thromboses in the LDLT group and three also had biliary complications. The graft type did not affect the biliary complication rates. There were no biliary complications in two right lobe graft recipients, although there were Table 3. Biliary Complications in Each Biliary Reconstruction Groups
Biliary complications Biliary leaks Biliary strictures
Duct-to-duct (n ¼ 49)
Hepaticojejunostomy (n ¼ 35)
19 (38%) 13 6
7 (20%) 5 2
.08 .07 .07
KARAKAYALı, KıRNAP, AKDUR ET AL
3526 Table 4. Type of Treatment Modalities for Biliary Complications Duct-to-duct
Interventional radiology Abdominal drainage only Internal-external biliary drainage catheter Balloon dilatation for one session Multiple balloon dilatation ERCP Endoscopic Retrograde Cholangiopancreatography Stent Surgery Hepaticojejunostomy
Deceased Living Deceased donor donor donor (n ¼ 5) (n ¼ 44) (n ¼ 1)
Living donor (n ¼ 34)
12 complications in 36 left lobe grafts (33.3%), 12 complications in 40 left lateral segment grafts (30%), and two complications in six whole liver grafts (33.3%) were observed. In 19 of 26 patients, the biliary complications were successfully treated with interventional radiologic procedures and one was treated with stent placement during Endoscopic Retrograde Cholangiopancreatography ERCP. In six patients, surgery was required for treatment as other
Fig 1. In seven patients, bile leaks were successfully treated with internal-external biliary drainage catheter insertions by percutaneous route, in these cases bilioma due to leak was also drained by a pig-tale catheter.
methods failed; duct-to-duct anastomosis was converted to HJ in all of them (Table 4; Fig 1). DISCUSSION
Pediatric segmental liver grafts have relatively smaller sized vascular and biliary structures, which leads to higher complication rates. Although the optimal technique for biliary reconstruction in liver transplantation remains controversial and depends on the experience of the surgical team, most centers prefer to use the Roux-en-Y HJ if the recipient is in the pediatric age group.4 In patients who have biliary atresia or who have had prior HJ operation, the Roux-en-Y technique is mandatory. But in patients with an available extrahepatic biliary system, the chance of duct-toduct anastomosis should be evaluated because duct-to-duct anastomosis has certain advantages compared to HJ, such as lower intra-abdominal contamination risk from the gastrointestinal system, early return of gastrointestinal motility, shorter operation time, and shorter stay in the intensive care unit. It is also a physiologic procedure preserving the Oddi sphincter and provides the chance of endoscopic interventions in the post-transplantation period when necessary.3,7 In some previous studies, duct-to-duct anastomosis was accepted as a contraindication in left lobe grafts as the authors claimed that the arterial supply of the central portion of the left hepatic duct came from the right hepatic artery which made the left biliary ducts more vulnerable to ischemia.10 However, in time, some reports existed showing acceptable low complication rates with duct-to-duct anastomosis in left lobe grafts.5e7 In our series, we preferred to perform a duct-to-duct anastomosis whenever it was possible, even for grafts with multiple ducts. Although the reason for early stenosis which occurs in the ﬁrst month post-transplantation is usually a technical error, late strictures are often caused by an impaired blood supply.3 It is well known that hepatic arterial complications may cause featuring biliary complications. In our series, in nine recipients with hepatic arterial problems, three also had concomitant biliary complications. The complication rate was not found to be higher than the patients without arterial insufﬁciency. In our previous studies, we reported similar biliary complication rates between duct-to-duct anastomosis and HJ.11 As the number of patients increased in both groups, some differences appeared in complication rates in favor of the HJ group. However, the difference is statistically insigniﬁcant. Regardless of the biliary reconstruction technique used, experienced interventional radiology or ERCP teams have extremely important roles in the management of biliary complications which can save most of the patients from reoperations and even from retransplantations. In our series, only 6 of 26 patients underwent a surgery. Leaks from the anastomosis site can be treated successfully using
internal, external, or internal plus external biliary stents. However, the leak may cause additional smaller intrahepatic ducts than normal, making percutaneous drainage more difﬁcult. Strictures can be treated by balloon dilatations and stent placements by percutaneous or endoscopic routes whenever necessary. Besides, the biliomas can be drained under the guidance of ultrasonography. Although ERCP is the primarily preferred method for treatment of biliary complications especially in patients with duct-to-duct anastomosis, it is not always available, particularly if the pediatric recipient is in question as the procedure requires special small caliber devices. In our center, the percutaneous radiological interventions have become the preferred treatment modality for pediatric recipients, even in duct-to-duct reconstructions, after having cannulation problems of the bile ducts proximal to the leak site during ERCP. The reported biliary stricture rates differ from 3% to 6%, and some large series have reported higher stricture rates after HJ compared to duct-to-duct anastomosis.12 We observed eight strictures, six in the duct-to-duct group and two in the HJ group; both groups can be treated without surgery. Most strictures require more than one intervention with balloon dilatation and/or stent placement. In conclusion, percutaneous interventional procedures are valuable, effective, and life-saving therapeutic alternatives for the treatment of bile leaks and strictures after PLTs. These procedures may be performed with high technical success rates, even in serious biliary complications.
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