LIVER TRANSPLANTATION 20:347–354, 2014

ORIGINAL ARTICLE

Single-Center Experience and Long-Term Outcomes of Duct-to-Duct Biliary Reconstruction in Infantile Living Donor Liver Transplantation Hidekazu Yamamoto, Shintaro Hayashida, Katsuhiro Asonuma, Masaki Honda, Hiroko Suda, Takahiro Murokawa, Yuki Ohya, Kwang-Jong Lee, Takayuki Takeichi, and Yukihiro Inomata Department of Transplantation and Pediatric Surgery, Postgraduate School of Medical Science, Kumamoto University, Kumamoto, Japan

The indications for duct-to-duct (DD) biliary reconstruction in living donor liver transplantation (LDLT) for small children are still controversial. In this study, the feasibility of DD biliary reconstruction versus Roux-en-Y (RY) biliary reconstruction was investigated in terms of long-term outcomes. Fifty-six children who consecutively underwent LDLT with a weight less than or equal to 10.0 kg were enrolled. Biliary reconstruction was performed in a DD fashion for 20 patients and in an RY fashion for 36 patients. During a minimum follow-up of 2 years, the incidence of biliary strictures was 5.0% in the DD group and 11.1% in the RY group. Cholangitis during the posttransplant period was observed in the RY group only. There were no deaths related to biliary problems. This study shows that DD reconstruction in LDLT for small children (weighing 10.0 kg or C 2014 AASLD. less) is a feasible option for biliary reconstruction. Liver Transpl 20:347-354, 2014. V Received September 27, 2013; accepted December 4, 2013. Liver transplantation is the only effective treatment for end-stage liver disease. Although considerable progress has been achieved and the surgical techniques have been refined for living donor liver transplantation (LDLT), the incidence of biliary complications remains significant. Duct-to-duct (DD) choledochocholedochostomy for biliary reconstruction is currently accepted as a standard method for adult recipients.1-3 DD reconstruction has several advantages over Roux-en-Y (RY) reconstruction: it is simpler and faster to perform without intestinal manipulation, it helps to maintain the physiological bilioenteric continuity by preserving the function of the sphincter of Oddi, it leads to an earlier start of oral intake, and it facilitates the management of endoscopic treatment in cases with postoperative biliary complications.4-6 Furthermore, dehiscence of an RY anastomosis can be fatal because it may be associated with septic peritonitis.

Greif et al.7 reported that biliary leakage in an RY anastomosis was associated with a higher rate of mortality (54.5%) than biliary leakage in a DD anastomosis (8.5%). However, in pediatric recipients, RY hepaticojejunostomy is the dominant method used for biliary reconstruction because the most common indication is biliary atresia. The application of a DD anastomosis is still controversial and is limited in pediatric LDLT. Several programs have reported that DD biliary reconstruction leads to more biliary complications in comparison with RY hepaticojejunostomy, especially in small infants weighing less than 10 kg.8,9 In our experience, however, DD reconstruction for pediatric cases, including infants, has led to excellent outcomes during the short-term follow-up period.10,11 In the present study, long-term outcomes were evaluated for DD biliary reconstruction versus RY hepaticojejunostomy in pediatric recipients with a body weight less than 10 kg at the time of transplantation.

Abbreviations: 3D-DIC, 3-dimensional drip infusion cholangiography; ALT, alanine aminotransferase; CT, computed tomography; DD, duct-to-duct; gGTP, gamma-glutamyl transpeptidase; GRWR, graft-to-recipient weight ratio; LDLT, living donor liver transplantation; NS, not significant; RY, Roux-en-Y. The authors have no conflicts of interest to disclose regarding this article. Address reprint requests to Hidekazu Yamamoto, M.D., Ph.D., Department of Transplantation and Pediatric Surgery, Postgraduate School of Medical Science, Kumamoto University, 1-1-1, Honjo, Chuo-Ku, Kumamoto 860-8556, Japan. Telephone: 181-96-373-5616; FAX: 181-96-3735783; E-mail: [email protected] DOI 10.1002/lt.23819 View this article online at wileyonlinelibrary.com. LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseases

C 2014 American Association for the Study of Liver Diseases. V

348 YAMAMOTO ET AL.

PATIENTS AND METHODS Patients The study protocol received a priori approval from the appropriate institutional review committee. One hundred twenty-nine LDLT procedures for pediatric patients under the age of 18 years were performed at Kumamoto University from 1999 to 2012. Sixty-three recipients weighed less than 10 kg at the time of LDLT. Fifty-six of these patients who were followed for 2 years or more were enrolled in this study, and their outcomes were analyzed through reviews of their clinical records. The eligible patients included 26 males and 30 females with a median age of 8.0 months (range 5 0.4 to 45 months), a median body weight of 6.9 kg (range 5 2.610.0 kg), and a median Pediatric End-Stage Liver Disease score at the time of transplantation of 14.0 (range 5 26 to 50). Forty-five children (80.4%) were under the age of 1 year at the time of transplantation. The original diseases of the recipients were biliary atresia (n 5 33), metabolic disease (n 5 10), fulminant hepatic failure (n 5 5), hepatoblastoma (n 5 3), Alagille syndrome (n 5 2), Byler disease (n 5 1), cryptogenic liver cirrhosis (n 5 1), and neonatal hemochromatosis (n 5 1). The minimum follow-up period was 2 years, and the median follow-up was 66 months.

Preoperative Evaluation of the Donors Donor candidates were forwarded to medical screening consisting of blood group tests, blood tests, abdominal ultrasonography, and other tests for systemic diseases. The final candidates were examined with computed tomography (CT) to assess the hepatic volume and anatomical configuration of vessels and bile ducts. The biliary anatomy was assessed through the 3-dimensional reconstruction of CT images by enhancement with the drip infusion of a contrast dye [3-dimensional drip infusion cholangiography (3D-DIC) CT].

Operation During the donor surgery, the findings of 3D-DIC CT were used, and the hepatic duct was sharply transected with surrounding connective tissue of the hilar plate after confirmation of the appropriate site with intraoperative cholangiography. Bleeding from periductal small arteries was controlled by suturing (but not by coagulation). Histidine-tryptophan-ketoglutarate was used as the perfusion and storage solution. The surgical procedure for the recipients was described previously.10-12 In cases with conditions other than biliary atresia, DD reconstruction was primarily considered. At this moment, we do not have absolute criteria for contraindications to DD for non–biliary atresia cases; however, if the wall of the native bile duct is too fragile, even with the finest 7-0 stitches, or if a 3-Fr stent catheter cannot be passed through the native common bile duct, we may choose to stop the DD procedure. The recipient’s bile duct was transected above the bifurcation preserving as much of the connective tissue around the duct as

LIVER TRANSPLANTATION, March 2014

possible. After implantation of the graft, the graft hepatic duct was reconstructed after the reconstruction of the hepatic vein, portal vein, and hepatic artery. Size matching with the graft’s duct was considered when we chose the reconstruction site for the recipient. The anastomosis was performed under a surgical loupe (32.5) with interrupted sutures of 6-0 absorbable polydioxanone monofilament. Individual sutures were placed with an interval of approximately 1 mm between stitches. The interrupted sutures were placed and tied so that the knots were outside the lumen of the anastomosis. An external biliary stent tube (3- or 4-Fr polyethylene tube) was placed across the anastomosis. The biliary tube was passed through the choledochal wall or the stump of the cystic duct or the other stump of the hepatic duct that was not used for the anastomosis, and then it was passed outside the abdomen. In RY reconstruction, the RY jejunal limb was anastomosed to the graft hepatic duct in an end-to-side fashion. The RY jejunal limb previously created during the Kasai operation was used, or an RY limb was newly created when DD reconstruction had to be abandoned for reasons other than biliary atresia. Hepaticojejunostomy was performed with anterior and posterior interrupted sutures of 6-0 absorbable polydioxanone monofilament. A 4-Fr transanastomotic tube was routinely exteriorized with the Witzel maneuver. Postoperative cholangiography via the external biliary stent tube was performed to rule out biliary stenosis or leakage 1 month after transplantation. The stent tube was kept in place for at least 3 to 6 months, after which it was removed at the outpatient clinic. If the patient developed a fever after removal, intravenous antibiotics were administered.

Postoperative Evaluation of the Recipients and Definition of Biliary Complications Bile leakage was defined as the observation of leakage during the postoperative cholangiography evaluation, persistent biliary drainage fluid from the postoperative drainage tube, or significant peritoneal fluid collection that was drained and confirmed to be bile. Bile strictures were suspected on the basis of biochemical examinations, elevated serum hepatobiliary enzyme levels, and/or total bilirubin levels. Abdominal ultrasonography, 3D-DIC CT, and hepatobiliary scintigraphy were used for the detection of biliary stenosis. Direct cholangiography, such as percutaneous transhepatic cholangiography or endoscopic retrograde cholangiography, was performed when it was needed and it was possible to confirm a biliary stricture. In this study, any abnormality that needed treatment was counted as a biliary stricture. Cholangitis was defined as the presence of a fever, elevated bile duct enzymes, and elevated inflammation parameters.

Statistical Analysis The results are expressed as means and standard deviations. Continuous data were analyzed with the

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Mann-Whitney test, and categorical variables were evaluated with the v2 test and Fisher’s exact test. A P value < 0.05 was considered to be statistically significant. All statistical analyses were carried out with the SPSS 18 statistical software program (IBM, Japan).

RESULTS DD reconstruction was performed for 20 patients, whereas RY hepaticojejunostomy was performed for 36 patients. The demographic characteristics of the patients are presented in Table 1. The mean age of the recipients at the time of transplantation was 10.3 months. Fourteen patients (70.0%) were less than 12 months old in the DD group, whereas 31 patients (86.1%) were less than 12 months old in the RY group. In the DD group, the mean body weight was 6.9 kg, the minimum weight was 2.6 kg, and the body weight was less than 6 kg in 6 cases. In the RY group, the mean body weight was 7.0 kg, and the body weight was less than 6 kg in 8 cases. There were no significant differences in the recipient age, recipient body weight, or donor age. The rate of biliary atresia cases versus non–biliary atresia cases in the RY group

was higher than the rate observed in the DD group. In the RY group, 3 non–biliary atresia cases were included: 1 with DNA depletion syndrome and 2 with Alagille syndrome. DD could not be performed in these cases because the caliber of the hepatic duct of the recipient was too small. The wall of the hepatic duct was easily torn with 7-0 stitches with a needle, and a 3-Fr catheter could not be passed through the hepatic duct. The surgery-related variables are listed in Table 2. The length of the operation and the cold ischemia time were significantly shorter for the DD group versus the RY group. The graft-to-recipient weight ratios (GRWRs), the graft weights, and the warm ischemia times were similar for the 2 groups. For half of the recipients with DD, the left lateral segment was reduced.

Surgical Procedures for DD Choledochocholedochostomy and RY Hepaticojejunostomy Among the patients treated with a DD anastomosis, there were 2 orifices of the bile duct in the graft in 1

TABLE 1. Demographic Characteristics of the Patients Characteristic Age (months)* Body weight (kg)* ABO incompatibility [n (%)] Donor age (years)* Original disease [n (%)] Biliary atresia Metabolic disease Fulminant hepatic failure Hepatoblastoma Byler disease Cryptogenic cirrhosis Neonatal hemochromatosis Alagille syndrome

DD Patients (n 5 20)

RY Patients (n 5 36)

P Value

10.3 6 9.8 (0.4 to 45 months) 6.9 6 2.0 (2.6-10.0) 4 (20) 30.6 6 3.4 (23-38)

8.7 6 4.2 (3-22) 7.0 6 1.4 (3.2-10.0) 7 (19.4) 32.4 6 7.6 (23-62)

NS NS NS NS

Single-center experience and long-term outcomes of duct-to-duct biliary reconstruction in infantile living donor liver transplantation.

The indications for duct-to-duct (DD) biliary reconstruction in living donor liver transplantation (LDLT) for small children are still controversial. ...
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