The pre-Kasai procedure in living donor liver transplantation for children with biliary atresia

Chengdu, China

The pre-Kasai procedure in living donor liver transplantation for children with biliary atresia

Qiao Wang, Lu-Nan Yan, Ming-Man Zhang, Wen-Tao Wang, Ji-Chun Zhao, Cong-Lun Pu, Ying-Cun Li and Quan Kang

Chengdu, China

BACKGROUND:Biliary atresia (BA) is a major cause of chronic cholestasis, a fatal disorder in infants. This study was undertaken to evaluate the safety and effectiveness of primary living donor liver transplantation (LDLT) in comparison with the traditional fi rst-line treatment, the Kasai procedure.

METHODS:We assessed 28 children with BA at age of less than two years (3-21.3 months) who had undergone LDLT in two hospitals in Southwest China during the period of 2008-2011. Eighteen children who had had primary LDLT were included in a primary LDLT group, and ten children who had undergone the Kasai operation in a pre-Kasai group. All patients were followed up after discharge from the hospital. The records of the BA patients and donors were reviewed.

RESULTS:The time of follow-up ranged 12-44.5 months with a median of 31 months. The 30-day and 1-year survival rates were 85.7% and 78.6%, respectively. There was no signif i cant difference in the 30-day or 1-year survival between the two groups (83.3% vs 90% and 77.8% vs 80%,P>0.05). The main cause of death was hepatic artery thrombosis. There were more patients with complications who required intensive medical care or re-operation in the pre-Kasai group (8, 80%) than in the primary LDLT group (9, 50%) (P=0.226). But no signif i cant differences were observed in operating time (9.3 vs 8.9 hours,P=0.77), intraoperative blood loss (208.6 vs 197.0 mL,P=0.84) and blood transfusion (105.6 vs 100.0 mL,P=0.91) between the two groups. The durations of ICU and hospital stay in the primary LDLT group and pre-Kasai group were 180.4 vs 157.7 hours (P=0.18) and 27 vs 29 days (P=0.29), respectively.

CONCLUSIONS:Primary LDLT is a safe and eff i cient management for young pediatric patients with BA. Compared with the outcome of LDLT for patients receiving a previous Kasai operation, a similar survival rate and a low rate of re-operation and intensive medical care for patients with BA can be obtained.

(Hepatobiliary Pancreat Dis Int 2013;12:47-53)

biliary atresia;living donor; liver transplantation; pediatric; Kasai operation

Introduction

Biliary atresia (BA) is a major cause of chronic cholestasis, a fatal congenital disorder in infants. The prevalence of BA is 1/20 000-1/8000 in live births.[1,2]The fi rst-line treatment is the Kasai procedure, fi rst reported in 1956.[3]Liver transplantation for BA began in 1967[4]and is currently recommended for patients who had a failed Kasai operation or who were unsuitable for this operation.

This strategy was based on the shortage of organ donors and a general concern about the safety of liver transplantation in infants. However, 30% of children with BA required liver transplantation in one year after the Kasai procedure,[5]indicating these children have to undergo liver transplantation at a considerably young age. More than 50% of children need transplantation before adulthood because of liver cirrhosis or other life-threatening problems.[6-9]Since techniques of transplantation have developed greatly during the past few years, and living donor liver transplantation (LDLT) has become an alternative to deal with organ shortage. Therefore, a question arises, i.e., can LDLT be performed primarily on patients with BA, without a previous Kasai operation as a "primary LDLT"? In the present study, 18 patients with BA under the age of twoyears who had undergone primary LDLT were followed up to examine the feasibility and safety of this practice in comparison with ten patients who had undergone the Kasai operation.

Methods

Twenty-eight patients who had received liver transplantation at West China Hospital, Sichuan University and Children's Hospital of Chongqing Medical University from January 2008 to January 2011 were evaluated. All patients aged less than two years (mean age 7.5 months) underwent LDLT. Eighteen patients (primary LDLT group) received primary LDLT immediately after the diagnosis of BA, which was conf i rmed by Doppler sonography, CT scan, or intraoperative choledochoscopy. Indications for transplantation were age ≥3 months with PELD ≥10 (four patients failed to meet the criteria of PELD score received LDLT). Ten patients who had had a Kasai operation (pre-Kasai group) underwent LDLT due to inadequate bile drainage and progressive deterioration of liver function. All the patients were followed up after discharge. The records of these BA patients and their donors were retrospectively reviewed.

Operative technique

The graft consisted of the left lateral segment (segments II & III) in 27 donors and segment II in one donor. Graft angioplasty was performed if necessary. Cholecystectomy was performed in 18 donors, and cholangiography was done via the cystic duct afterwards. Cholangiography was performed in other donors via fi ne needle puncture of the common hepatic duct without cholecystectomy. The ostia of the left, middle, and right hepatic veins of the recipients were reconstructed to form a common opening to anatomize with the graft hepatic vein. The remnants of the left and right portal veins of the recipients were dissected and reconstructed to form an umbrella-like opening to adjust to the end-to-end anatomosis with the graft portal vein. A similar procedure was done with the hepatic artery of the recipients using microsurgical techniques after reperfusion of the hepatic and portal vein. Duct-to-jejunum Roux-en-Y biliary reconstruction was performed with interrupted suturing by using 7-0 prolene without biliary stent implantation. Intraoperative color fl ow Doppler ultrasound was performed after vessel anatomosis and abdomen closure to assure that the blood fl ow was lucid.

Immunosuppression

All the patients who had had LDLT received cyclosporine (Novartis, Basel, Switzerland) combined with methyprednisolone as a primary immunosuppressive therapy. Cyclosporin was given orally to reach a serum concentration of 250-350 ng/mL 12 hours after last intake (C0), which was gradually reduced to 100-200 ng/mL for maintenance. Methyprednisolone was administrated intravenously (3 mg/kg per day during the fi rst 1-2 postoperative weeks). Later, it was replaced by oral administration of prednisolone (2.5 mg/kg per day then tapered). Steroids were withdrawn within one to three months. Mycophenolate (Roche, Basel, Switzerland) was used in six patients who were indicated for additional immunosuppressive treatment. The dosage of mycophenolate administrated and tapered was dependent on the results of liver function tests.

Follow-up

All the patients were followed up monthly in the fi rst postoperative year and every three months subsequently by outpatient service and by telephone interview. Medical records were reviewed to abstract information on height, weight, serum liver function tests (albumin, ALT, AST, alkaline phosphatase, gamma glutamate, transpeptidase, bilirubin), renal function (blood urea nitrogen, creatinine) , cholesterol, triglycerides, glucose, uric acid, hepatitis surveillance, complete blood count, blood concentration of immunosuppressive agents, and abdomen Doppler ultrasonography.

Statistical analysis

Statistical analyses were made with the software SPSS 13.0 (SPSS Inc., Chicago, IL., USA). Survival was def i ned as the time between the day of transplantation and the end of February 2011 or patient death. Graft survival was def i ned as the time between the day of transplantation and the time of re-transplantation or patient death. The preoperative status and the outcomes of transplantation were compared using Student'sttest. The prevalence of preoperative diseases and postoperative complications was compared with Fisher's exact test. Kaplan-Meier survival estimates and differences between curves were tested using the logrank test. APvalue of <0.05 was considered statistically signif i cant.

Results

Recipients

In the 28 recipients (Table 1), 12 were male and 16 female, of whom nine were under 6 months old. The average age of the patients in the pre-Kasai and primaryLDLT groups were 8.4 and 7 months, respectively (P=0.36). The mean weight of the patients was 7.1 kg in both groups. The patients in the pre-Kasai group underwent the Kasai procedure 2-9 months before LDLT and three of them were found to have cholangitis, a common complication requiring preoperative antibiotic treatment. Liver cirrhosis was detected in most (78.6%) of the patients by sonography or biopsy and showed no statistically signif i cant difference between the two groups. Splenomegaly of varied degrees was observed in these patients. One patient in the primary LDLT group was diagnosed with malnutrition. Thirteen (46.4%) patients experienced progressive jaundice during the preoperative period, and ten of them were in the primary LDLT group. The mean PELD scores of the patients at the time of transplantation were 11.9 and 16 in the pre-Kasai and primary LDLT groups, respectively (P=0.21). There was no signif i cant difference in preoperative factors between the two groups.

Table 1.Preoperative status of the recipients of the pre-Kasai and primary LDLT groups

Patient survival

The follow-up duration ranged from 12 to 44.5 months with the median of 31 months. The life curves of the two groups are shown in Fig. 1. The overall survival rates of patients and grafts at the fi rst 30 postoperative days were both 85.7%. The 6-month and 1-year survival rates were 78.6% and 78.6%. The life curves of the two groups showed similar patterns without statistically signif i cant difference. In the pre-Kasai group there were two deaths, one occurred on the 14th postoperative day due to hepatic artery thrombosis and the other was due to severe rejection. In the primary LDLT group, two patients died of hepatic artery thrombosis on the 14th and 20th postoperative days, one of which had had re-transplantation 3 days after a previous operation. Another in-hospital death in the primary LDLT group occurred on the 21st day after LDLT because of accidental choking during breast feeding. One patient in this group was found to have hepatic vein stenosis 4 months after LDLT and experienced fatal ventricular fi brillation after hepatophlebography.

Fig. 1.Kaplan-Meier survival curves of the 28 patients of the pre-Kasai and primary LDLT groups (P=0.89).

Table 2.Short- and long-term postoperative complications of the recipients

Complications

The life threatening complications (Table 2) included hepatic artery thrombosis and/or hematoma in 4 patients (14.3%), subdiaphragmatic abscess in 2 (7.1%), adhesive intestinal obstruction in 2 (7.1%), abdominal hemorrhage in 3 (10.7%), and intestinal perforation in 4 (14.3%). None of the patients had biliary stricture. Mild complications included pneumonia in 7 (25%) patients who required antibiotic treatment and mild rejection in 3 (10.7%) patients.

Re-transplantation was performed for one patient of the primary LDLT group, who had hepatic artery thrombosis three days after the operation. The patient died from acute liver dysfunction seven days later. The patients who experienced the same complication died before re-transplantation. The patient with hepatic arterial hematoma received vessel dilation and anticoagulation treatment after intrahepatic angiography and recovered uneventfully.

Complications beyond 30 postoperative days included hepatic vein stenosis four months after transplantation, which led to the death of a patient and upper gastrointestinal hemorrhage in another patient 28 months after the operation by portal-azygous disconnection with splenectomy. One patient in the pre-Kasai group suffered from cholangitis after transplantation and was treated conservatively for 6 months.

Operation

The operative characteristics of transplantation are shown in Table 3. The graft weight and GRWR were relatively lower in the primary LDLT group (234.7 g vs 279.5 g, and 3.4% vs 3.9%, respectively). The mean intraoperative blood loss was 197 mL and 208.6 mL in the pre-Kasai and primary LDLT groups, respectively (P=0.84). Six patients in the pre-Kasai group and 11 in the primary LDLT group required blood perfusion. The mean volumes of pack red cells were 100 mL and 105.6 mL in the pre-Kasai and primary LDLT groups, respectively (P=0.91). All patients required vessel reconstruction of the hepatic artery, hepatic vein and portal vein to adjust to differences between recipients and donors. The mean operative time was 8.9 and 9.3 hours in the pre-Kasai and primary LDLT groups, respectively. One patient with intraoperative portal vein thrombosis in the primary LDLT group required thromboectomy, which prolonged the operative time to 24.7 hours. There was no signif i cant difference in hospitalization and ICU stay between the two groups.

Donors

The twenty-eight donors included 14 mothers (50%), 10 fathers (35.7%), 3 grandmothers (10.7%), and 1 cousin (3.6%) (Table 4). Their mean age was 32.5 years. In these donors, the mean operative time was 6.1 hours, and the mean intraoperative blood loss was 261.5 mL. Their mean ICU stay and hospital stay were 5 and 17 days, respectively. One donor had portal vein thrombosis during the post-operative period, which was treated conservatively. Other donors recovered uneventfully after the operation.

Table 4.Donor characteristics and operative outcome (n=28)

Discussion

At the Annual Meeting of American College of Surgeons in 1985, Drs. Starzl and Gordon[10]stated that liver transplantation is made immeasurably more diff i cult by the Kasai operation prior to transplantation. However, this statement was not widely accepted in the fi eld of pediatric liver transplantation for BA because of the following considerations:[11]1) shortage of organ supply and the interminable time the patients are on the waiting list for transplantation; 2) complexity of surgery on infants; 3) potential long-term palliation or even treatment with a Kasai operation alone. The concepts of "keeping the function of the native liver" and "avoiding the possibility of transplantation" were commonly followed by most surgeons.[5]The development of LDLT has made pediatric liver transplantation different, as this operation can be an alternative for the shortage of organs from deceased donors and shorten the waiting time. Furthermore, the quality of the organ can be ensured by preoperative examinations.

No signif i cant differences were observed between the two groups in operative time, blood loss, and blood transfusion, which were contradictory to the report by Sandler et al.[11]This may be due to the improvementof surgical techniques in the past years. Clinically, abdominal adhesion after the Kasai operation may lead to diff i culty in transplantation, especially for pediatric patients.[12-15]In our center, the hepatic artery and bile duct are usually anastomosed microsurgically to improve their patency. The mismatch of the size of vessels between adult donors and infant recipients may lead to more complicated anastomosis of vessels than in adult-to-adult LDLT. In our patients, the hepatic veins, hepatic arteries, and portal veins were reconstructed in all patients.

Complications above grade III of Clavien classif i cation[16]included hepatic arterial hematoma, hepatic artery thrombosis, subdiaphragmatic abscess, adhesive intestinal obstruction, intra-abdominal hemorrhage, intestinal perforation, rejection, hepatic vein stenosis and upper gastrointestinal hemorrhage. In our study, patients with complications who required intensive medical care or re-operation in the pre-Kasai group were more than those in the primary LDLT group. Hepatic artery thrombosis was considered the most signif i cant risk for graft loss and increased mortality.[17,18]In our study, its prevalence was 10.7% which is higher than that reported elsewhere.[18-20]Vascular complications vary in different series of pediatric LDLT, in which portal vein thrombosis comprises the majority, with a prevalence of 8%-17%.[18,19,21]Portal vein hypoplasia, which is common in patients with BA, is an important risk factor for post-transplant thrombosis.[22,23]One portal vein thrombosis was detected in our series although portal vein hypoplasia was seen by biopsy in most patients. Biliary complications including cholangitis, bile leak, and biliary stricture were frequently reported.[17,20,24]No bile leak was seen in our series, and only one patient in the pre-Kasai group had cholangitis and slight biliary stricture postoperatively. The patient wastreated conservatively. Rejection is a potentially lethal complication after liver transplantation.[25]In our series, the total rejection rate was 14.3%. Three patients had mild rejection in the acute phase and were treated with immunosuppressive agents. Another patient had more severe rejection 6 months after LDLT and one patient died before re-transplantation. Scholars[26]reported that the survival rate of primary LDLT for infants with BA is up to 90%-95%, which is similar to that of the Kasai procedure. However, this remains a challenge for transplant surgeons.

Table 5.Base-line characteristics and outcome of Kasai group and primary LDLT group

In our series, the postoperative and 1-year survival rates were 85.7% and 78.6%, and their average age at transplantation was 7.5 months. The survival rates were comparable with the 1-year survival rate of 75% reported by Venick et al whose patients were 9 months old on average.[14]In their retrospective analysis of more than 200 patients, age less than 6 months was considered as a signif i cant predictor for poor outcomes. Kanazawa et al[27]reported a 1-year survival of 88.2% after LDLT for infants with BA, suggesting that portal vein reconstruction may improve the outcome.

The potential of palliation by the Kasai operation should not be underestimated. In noted centers, 60% of pediatric patients had biliary drainage after Kasai portoenterostomy.[5]A recent study on long-term results of the Kasai operation showed 5-, 10-, and 20-year survival rates of patients with their native livers of 63%, 54%, and 44%.[28]The results also showed that a high concentration of bilirubin, a longer duration of jaundice before the Kasai operation, phototherapy in the neonatal period, and ductules smaller than 200 μm might suggest the poor outcome of Kasai operation and a need for transplantation.[6,29]In our study, we further compared the results of the primary LDLT group with those of 33 patients who underwent Kasai operation as the primary treatment (Table 5). All patients in the primary LDLT group who survived at least 30 days were free from jaundice. However, 70.4% of the patients who survived at least 30 days in the Kasai group were jaundice free (P=0.035). Although a favorable result was found in the primary LDLT group, the life curves (P=0.253) and 30-day (P=1) and 1-year survival rates (P=0.352) did not show any statistical differences (Fig. 2). The main causes of death were pneumonia and liver malfunction with severe ascites (69%). Other causes included intracranial hypertension, primary neoplasm, intestinal obstruction, and upper gastrointestinal hemorrhage. Patients in the Kasai group were signif i cantly younger than those in the primary LDLT group (P=0.000). PELD scores in the primary LDLT group were higher than that in the Kasai group (P=0.001). Studies have suggested that age>3 months[30]is an important prognostic factors for the poor outcome after Kasai operation. And by studying the 33 patients who received Kasai operation as the primary treatment, PELD score >10 had a signif i cant impact on the poor outcome after Kasai operation, too (P=0.018). Hence, LDLT can be used as the fi rst-line treatment for those who aged more than 3 months and PELD score above 10. Further studies are needed to def i ne the indications for primary LDLT.

Fig. 2.Kaplan-Meier survival curves of the patients of the primary LDLT and Kasai groups (P=0.253).

Donor safety has always been a focus in LDLT. In our study, one complication in a donor was treated conservatively. As the recipients for primary LDLT were mostly infants, a graft consisting of the left lateral segment or even segment II was considered suff i cient. The GV/SLV ratio of the donors was 23% in the Kasai group and 23.9% in all donors, which were signif i cantly lower than the reported safety threshold of 60%.[31]

In conclusion, primary LDLT is safe and effective for young pediatric patients with BA. Compared with the results of LDLT for patients who have undergone a Kasai operation, a similar survival and a low rate of re-operation for complications can be expected. LDLT, as the fi rst-line treatment, may be more superior than the Kasai procedure in increasing the survival rate of patients. Hence, primary LDLT may be used as an alternative therapy for young pediatric patients with BA.

Contributors:YLN and ZMM proposed the study. WQ wrote the fi rst draft and analyzed the data. All authors contributed to the design and interpretation of the study and to further drafts and all of them participated in the operations of the patients. YLN is the guarantor.

Funding:This work was supported by a grant from the National Science and Technology Major Project of China (2008ZX10002-025 & 2008ZX10002-026).

Ethical approval:This study was approved by the Ethics Committee of the hospital.

Competing interest:No benef i ts in any form have been received or will be received from any commercial party related directly or indirectly to the subject of this article.

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Received November 27, 2011

Accepted after revision June 19, 2012

Lu-Nan Yan, MD, PhD, Liver Transplantation Division, Department of Surgery, West China Hospital, Sichuan University, Chengdu 610041, China (Tel: 86-28-85422867; Email: yanlunan688@163. com)

10.1016/S1499-3872(13)60005-3

AuthorAff i liations:Liver Transplantation Division, Department of Surgery, West China Hospital, Sichuan University, Chengdu 610041, China (Wang Q, Yan LN, Wang WT and Zhao JC); Department of Hepatobiliary Surgery, Children's Hospital, Chongqing Medical University, Chongqing 400014, China (Zhang MM, Pu CL, Li YC and Kang Q)

? 2013, Hepatobiliary Pancreat Dis Int. All rights reserved.