Single-Center Experience and Long-Term Outcomes of Duct-to-Duct Biliary Reconstruction in Infantile Living Donor Liver Transplantation
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1 LIVER TRANSPLANTATION 20: , 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 less) is a feasible option for biliary reconstruction. Liver Transpl 20: , VC 2014 AASLD. Received September 27, 2013; accepted December 4, 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 , Japan. Telephone: ; FAX: ; yamahide@fc.kuh.kumamoto-u.ac.jp DOI /lt View this article online at wileyonlinelibrary.com. LIVER TRANSPLANTATION.DOI /lt. Published on behalf of the American Association for the Study of Liver Diseases VC 2014 American Association for the Study of Liver Diseases.
2 348 YAMAMOTO ET AL. LIVER TRANSPLANTATION, March 2014 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 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 to 45 months), a median body weight of 6.9 kg (range kg), and a median Pediatric End-Stage Liver Disease score at the time of transplantation of 14.0 (range 526 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 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,ifthewallofthenativebileductistoofragile,even with the finest 7-0 stitches, or if a 3-Fr stent catheter cannotbepassedthroughthenativecommonbileduct, 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 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
3 LIVER TRANSPLANTATION, Vol. 20, No. 3, 2014 YAMAMOTO ET AL. 349 Mann-Whitney test, and categorical variables were evaluated with the v 2 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 DD Patients (n 5 20) RY Patients (n 5 36) P Value Age (months)* (0.4 to 45 months) (3-22) NS Body weight (kg)* ( ) ( ) NS ABO incompatibility [n (%)] 4 (20) 7 (19.4) NS Donor age (years)* (23-38) (23-62) NS Original disease [n (%)] <0.05 Biliary atresia 0 (0) 33 (91.7) Metabolic disease 9 (45) 1 (2.8) Fulminant hepatic failure 5 (25) 0 (0) Hepatoblastoma 3 (15) 0 (0) Byler disease 1 (5) 0 (0) Cryptogenic cirrhosis 1 (5) 0 (0) Neonatal hemochromatosis 1 (5) 0 (0) Alagille syndrome 0 (0) 2 (5.6) *The data are presented as means and standard deviations (with ranges in parentheses). TABLE 2. Surgery-Related Variables Variable DD Patients (n 5 20) RY Patients (n 5 36) P Value GRWR (%)* ( ) ( ) NS Graft weight (g)* (98-290) ( ) NS Length of the operation (minutes)* ( ) ( ) <0.01 Cold ischemia time (minutes)* (12-183) (28-234) <0.01 Warm ischemia time (minutes)* (33-59) (31-163) NS Graft type [n (%)] NS Lateral 10 (50) 27 (75) Reduced lateral 10 (50) 9 (25) Multiple bile duct orifices in the graft [n (%)] 1 (5) 0 (0) NS Multiple biliary reconstructions [n (%)] 1 (5) 0 (0) NS *The data are presented as means and standard deviations (with ranges in parentheses).
4 350 YAMAMOTO ET AL. LIVER TRANSPLANTATION, March 2014 case only. These 2 orifices were separately anastomosed. Therefore, there were actually 21 biliary anastomoses in this series. The most common anastomotic site in the recipient was a branch patch or united orifices of the left and right hepatic ducts of the recipient. It was followed by the stump of the common hepatic duct. The stumps of the left, right, and cystic ducts were also used in 1 case each. In only 1 case with double anastomoses, bile duct of Segment 2 (B2) and bile duct of Segment 3 (B3) in the graft were anastomosed to the cystic duct and the common hepatic duct, respectively. The DD anastomoses in 19 cases were performed with interrupted sutures, and the other case was treated with interrupted sutures for the anterior wall after continuous suturing of the posterior wall. An external transanastomotictubewasinsertedfromthestumpofthecystic duct in 14 patients, through the common bile duct in 5 patients, and via the stump of the right hepatic duct in 1 patient. The patient with 2 DD anastomoses received 2 transanastomotic tubes separately via the common bile duct. All RY anastomosis procedures included 1 hole end-to-side hepaticojejunostomy. Incidence of Biliary Complications No patients developed hepatic artery thrombosis. The biliary complications observed in the 2 groups are presented in Table 3. In the immediate postoperative period, biliary leakage was not encountered in any DD recipients. No cholangitis was observed during the follow-up period. One patient developed a biliary stricture 1.5 months after the transplant and underwent a conversion from a DD anastomosis to an RY anastomosis 8 months after LDLT after percutaneous transhepatic cholangiodrainage. The exact site of the biliary stricture in this case was the graft bile duct proximal to the biliary anastomosis, and it was confirmed with a cholangiogram (Fig. 1). In the RY group, biliary leakage was detected in 3 patients. The median onset of biliary leakage in the RY group was 14 days (range to 1.5 months) after LDLT. One patient had a persistent bilious discharge with high amylase and total bilirubin levels and was treated with RY diversion because of isolation of the biliary anastomosis from the regurgitation of intestinal juice. Cholangitis was identified in the RY group only (8 patients). Two of the 8 children presented with cholangitis within the first 6 months after LDLT, whereas 6 developed cholangitis more than 6 months after the operation. Two children experienced more than 2 repeat episodes of cholangitis. Four patients developed biliary strictures in the RY group. Among these 4 patients, the median onset of biliary strictures was 3 months after surgery (range 53.0 to 5.0 months). The rates of biliary strictures and biliary leakage were not significantly different between the 2 groups. The rate of cholangitis was significantly higher for the RY group versus the DD group, especially more than 6 months after the operation. The liver enzyme levels during the latest evaluation showed normal values in all surviving cases (Fig. 2). There were no significant differences between the 2 groups with the exception of serum bilirubin levels 2 and 7 years after transplantation. Available histological examinations of graft livers performed for 12 patients in the DD group (via protocol biopsy) at a median of 40.1 months (range months) after transplantation revealed no findings of bile duct stenosis (eg, ductal proliferation or pathological cholangitis). Figure 1. Percutaneous transhepatic cholangiography image of a case with a biliary stricture. B2 and B3 were separately drained. Both B2 and B3 were disrupted at the intrahepatic or proximal level. There was no communication between B2 and B3 at the time of percutaneous transhepatic cholangiography. TABLE 3. Biliary Complications Complication DD Patients (n 5 20) RY Patients (n 5 36) P Value Leakage [n (%)] 0 (0) 3 (8.3) NS Onset (months)* (0.5 to 1.5 months) Stricture [n (%)] 1 (5.0) 4 (11.1) NS Onset (months)* ( ) Cholangitis [n (%)] 0 (0) 8 (22.2) <0.05 Onset (months)* ( ) *The data are presented as means and standard deviations (with ranges in parentheses). Eleven times.
5 LIVER TRANSPLANTATION, Vol. 20, No. 3, 2014 YAMAMOTO ET AL. 351 Figure 2. Changes in posttransplant ALT, ggtp, and serum bilirubin levels after biliary reconstruction. Open circles represent levels for DD patients (n 5 20), and filled circles represent levels for RY patients (n 5 36). *P < 0.05 for DD patients versus RY patients. Survival The cumulative patient survival rates were 85.0% and 80% for the DD group and 97.2% and 94.1% for the RY group at 1 and 3 years, respectively. The patient survival rates did not differ significantly between the groups. Four patients died after LDLT with DD reconstruction. The original diseases for these patients were glycogen storage disease type IV in 2 cases (siblings), hepatoblastoma in 1 case, and fulminant hepatic failure in 1 case. The causes of death for these 4 patients were considered to be related to the original diseases and not related to the biliary reconstruction. The pretransplant condition of 2 of the 4 cases (1 patient with fulminant hepatic failure and 1 patient with glycogen storage disease type IV) was too poor with high Pediatric End-Stage Liver Disease scores (21 and 31, respectively). The patient with fulminant hepatic failure died of pneumonia and subsequent multiorgan failure. The origin of the fulminant hepatic failure was unclear. In the patient with glycogen storage disease type IV, cardiomyopathy, likely due to the original disease, progressed after surgery. The sibling of the patient who died also had glycogen storage disease type IV and exhibited progressive hypertrophic cardiomyopathy with pulmonary hypertension. The remaining patient who died had hepatoblastoma and died because of its recurrence. Therefore, the patient selection was not good even though there were no other ways to save them. Two patients treated with RY reconstruction died because of pneumonia and pulmonary hypertension. Two of the 16 surviving recipients who were treated with DD reconstruction underwent retransplantation after the original LDLT procedure (one after 9 years and the other after 3 years). The original indications were Byler disease for the first case and fulminant hepatic failure for the other. The reasons for graft failure in these 2 cases were chronic rejection and progressive liver fibrosis due to an unknown cause after RY conversion from DD reconstruction, respectively. The first case (Byler disease) underwent DD biliary reconstruction again for the retransplant 9 years after the initial LDLT procedure. In the second case, retransplantation was performed 2 years after RY conversion. After RY conversion, the patient experienced no episodes of cholangitis or biochemical cholestasis. His explanted first graft showed grade III liver fibrosis and greater than 60% steatosis; however, no cholestasis or ductular proliferation were observed. Therefore, we judged that the fibrosis was not related to the biliary stricture. In the RY group, 3 recipients underwent retransplantation at a median of 4 months (range 5 10 days to 28 months) after the first transplantation procedure. In 1 patient, the histological findings of the explanted liver confirmed the presence of hepatic fibrosis and biliary proliferation due to a biliary stricture. The follow-up period among the surviving recipients ranged from 2 to 12 years. Morphological Changes in DD Reconstruction During Long-Term Follow-Up CT cholangiography was performed for 12 of the 15 survivors (after the exclusion of the patient who had an RY conversion) at a median recorded time of 40.1 months (range months). Good patency of the biliary tree was confirmed by CT cholangiography for the 12 patients. None of the patients had dilatation of the intrahepatic duct. CT cholangiography for 3 patients demonstrated focal narrowing of the anastomosis (Fig. 3A). None of the focal narrowing was associated with clinical signs of a biliary stricture. The CT cholangiogram for the patient with 2 anastomoses revealed no stricture (including the anastomosis of the cystic duct). Two patients had deformities of the extrahepatic donor and recipient bile ducts related to graft liver regeneration and patient growth (Fig.
6 352 YAMAMOTO ET AL. LIVER TRANSPLANTATION, March 2014 Figure 3. 3D-DIC CT images after long-term follow-up. (A) Image taken 4 years after the transplant. There was focal narrowing at the anastomosis, but it was not clinically significant (arrowhead). (B) Image taken 9 years after the transplant. There was a deformed course of the extrahepatic duct (circle), but it had good patency. TABLE 4. Graft Regeneration in 2 Cases of Deformities of the DD Biliary Tract First Case Second Case Time of After Transplantation Time of After Transplantation Transplantation 8 Months 9 Years Transplantation 2 Months 5 Years Graft volume 260 g 280 cc 603 cc 115 g 205 cc 561 cc GRWR (%) B). Graft regeneration was confirmed with CT volumetry for these 2 cases (Table 4). However, no negative impact or clinical signs associated with these deformities were observed. DISCUSSION In LDLT for pediatric recipients, RY reconstruction has been dominant because the main indication has been biliary atresia. In fact, Sakamoto et al. 8 and Tanaka et al. 9 reported RY hepaticojejunostomy to be the preferred method because there was a higher incidence of biliary strictures in a DD reconstruction group. On the other hand, the evaluation of DD biliary reconstruction in pediatric LDLT has been reported in a relatively limited number of studies. 4,8,9,13 The incidence of posttransplant strictures in DD patients ranged from 9.3% to 36.8% in those previous reports. In the present study, RY reconstruction was not found to be superior to DD reconstruction. We observed the outcomes of children with a body weight less than 10 kg who were treated with DD reconstruction for a longer period after transplantation in comparison with those treated with RY reconstruction, and we observed more cases in comparison with previous studies. The results of DD reconstruction were satisfactory, with only 1 case having a stricture. That case had a stricture at the intrahepatic bile duct proximal to the anastomosis, that is, a nonanastomotic site. This might have been caused by a poor blood supply to the donor s bile duct due to a burn injury from coagulation during the transection of the hepatic parenchyma, as reported elsewhere. 11 Additionally, this recipient received an ABO-identical graft with a shorter cold ischemia time (ie, 29 minutes). There were no specific difficulties in performing hepatic artery reconstruction during the operation. In this case, conservative endoscopic treatment was not successful. In DD reconstruction, the possibility of treatment via endoscopy has been one of the reasons for its superiority over RY reconstruction. However, in small children, the endoscopic procedure is not easy, and this reason cannot be used to recommend DD reconstruction over RY reconstruction. The rate of biliary strictures in our current study was lower than that in other studies. 8,9 Biliary strictures after LDLT commonly occur within 2 years of transplantation. In this study, all patients were
7 LIVER TRANSPLANTATION, Vol. 20, No. 3, 2014 YAMAMOTO ET AL. 353 followed for more than 2 years. This means that the incidence in this series can be properly counted. Although it is difficult to identify the reason for the low incidence of strictures, the technical aspects of the biliary reconstruction and transanastomotic stenting may have contributed to the good outcomes. ABOincompatible liver transplantation carries a high risk of hepatic necrosis and intrahepatic biliary complications, including diffuse biliary strictures, in which the bile duct injury is related to an impaired arterial circulation secondary to the presence of antibodymediated vasculitis. Eleven children (4 patients in the DD group and 7 patients in the RY group) received ABO-incompatible grafts in our series; however, ABOincompatible liver transplantation is not related to biliary strictures in infants, as reported by Egawa et al. 14 In terms of the technical aspects for the recipients, the peribiliary connective tissue of both the graft hepatic duct and the recipient bile duct were preserved to maintain an adequate blood supply to the bile duct. In the recipient bile duct, there was a dilemma regarding the dissection and preservation of the connective tissue. The lengthening of the bile duct by meticulous dissection for a safer anastomosis with less tension had to be balanced with the preservation of the peribiliary connective tissue. In every case, the blood supply at the stump of the bile duct was confirmed by the presence of fresh bleeding at the stump. The use of a biliary stent tube has been the subject of controversy. An external stent tube was kept in place for at least 3 months in our series. Similarly, other series have reported that the use of a biliary stent tube or T-tube is useful for preventing biliary complications. 8,15 On the other hand, Haberal et al. 4 reported that DD reconstruction without a biliary stent was a safe technique. In the present cases, there was no anastomosis without a stent tube. The limited number of biliary strictures in our series might indicate that the stent tube did not negatively affect the outcome. We do not know the exact reason why the results in the present series were relatively good in contrast to the findings of previous reports. Another possible explanation is that the quality of the native duct was good in most cases because most of the patients in this series were noncirrhotic and noninfectious. Although the diameter in the native duct was thin, the wall was very flexible and nonsclerotic. In terms of long-term complications, we found that cholangitis was a more common biliary complication in the RY group and occurred 6 months after transplantation or later, whereas no cases of cholangitis were noted in the DD group. Providing corroborative data, Sand et al. 16 reported that destruction of the sphincter of Oddi by endoscopic sphincterotomy resulted in ascending contamination of the bile duct. Consequently, RY patients have a risk of cholangitis due to the same phenomenon. The results of a morphological analysis of DD reconstruction in small pediatric recipients after a longterm follow-up period have not been reported. In this series, we confirmed the findings with long-term CT cholangiography. All patients who underwent a CT examination, including the case with 2 anastomoses, were found to have good patency of the biliary anastomosis. Although some cholangiograms demonstrated slight anastomotic narrowing, we did not count them as having biliary strictures because there were no clinical symptoms, elevated levels of liver enzymes, or pathological findings such as cholangitis. Matthews et al. 17 reported the cases of 3 patients with biliary strictures after hepatectomy, and they illustrated the influence of hepatic regeneration on attempts at subsequent stricture repair. Liver regeneration can cause marked rotation and displacement of the hepatic hilum. The results of our study indicate that the biliary tract can exhibit some degree of deformity due to liver regeneration and the growth of the patient. This deformity was unrelated to any clinical symptoms (eg, cholangitis) and was not associated with changes in biochemical markers. We think that lower GRWR grafts with the left lateral lobe potentially have the possibility of displacement of the hilum to the right and caudal side due to greater graft regeneration in comparison with that observed in higher GRWR grafts. However, we demonstrated that the deformities of the biliary system occurred because of graft regeneration during a longer period in only 2 cases, and they were not crucial. Two limitations of our study deserve further comment: the retrospective nature and the small sample size. Prospective and multicenter studies are, therefore, needed to clarify the long-term clinical outcomes of DD reconstruction. Despite these limitations, we believe that this study provides useful information regarding the clinical outcomes of DD biliary reconstruction because, to the best of our knowledge, it includes the largest number of patients with DD reconstruction evaluated over a lengthy follow-up period. In conclusion, the long-term results of DD biliary reconstruction in pediatric LDLT for recipients with a body weight less than 10 kg were satisfactory. DD reconstruction should, therefore, be considered for more cases of LDLT, regardless of age or body weight. REFERENCES 1. Ishiko T, Egawa H, Kasahara M, Nakamura T, Oike F, Kaihara S, et al. Duct-to-duct biliary reconstruction in living donor liver transplantation utilizing right lobe graft. Ann Surg 2002;236: Kasahara M, Egawa H, Takada Y, Oike F, Sakamoto S, Kiuchi T, et al. Biliary reconstruction in right lobe livingdonor liver transplantation: comparison of different techniques in 321 recipients. Ann Surg 2006;243: Soejima Y, Taketomi A, Yoshizumi T, Uchiyama H, Harada N, Ijichi H, et al. Biliary strictures in living donor liver transplantation: incidence, management, and technical evolution. Liver Transpl 2006;12: Haberal M, Karakayali H, Atiq A, Sevmis S, Moray G, Ozcay F, Boyvat F. Duct-to-duct biliary reconstruction without a stent in pediatric living-donor liver transplantation. Transplant Proc 2011;43:
8 354 YAMAMOTO ET AL. LIVER TRANSPLANTATION, March Chang JH, Lee IS, Choi JY, Yoon SK, Kim DG, You YK, et al. Biliary stricture after adult right-lobe living-donor liver transplantation with duct-to-duct anastomosis: long-term outcome and its related factors after endoscopic treatment. Gut Liver 2010;4: Tada S, Yazumi S, Chiba T. Endoscopic management is an accepted first-line therapy for biliary complications after adult living donor liver transplantation. Am J Gastroenterol 2007;102: Greif F, Bronsther OL, Van Thiel DH, Casavilla A, Iwatsuki S, Tzakis A, et al. The incidence, timing, and management of biliary tract complications after orthotopic liver transplantation. Ann Surg 1994;219: Sakamoto S, Egawa H, Ogawa K, Ogura Y, Oike F, Ueda M, et al. The technical pitfalls of duct-to-duct biliary reconstruction in pediatric living-donor left-lobe liver transplantation: the impact of stent placement. Pediatr Transplant 2008;12: Tanaka H, Fukuda A, Shigeta T, Kuroda T, Kimura T, Sakamoto S, Kasahara M. Biliary reconstruction in pediatric live donor liver transplantation: duct-to-duct or Roux-en-Y hepaticojejunostomy. J Pediatr Surg 2010;45: Okajima H, Inomata Y, Asonuma K, Ueno M, Ishiko T, Takeichi T, et al. Duct-to-duct biliary reconstruction in pediatric living donor liver transplantation. Pediatr Transplant 2005;9: Shirouzu Y, Okajima H, Ogata S, Ohya Y, Tsukamoto Y, Yamamoto H, et al. Biliary reconstruction for infantile living donor liver transplantation: Roux-en-Y hepaticojejunostomy or duct-to-duct choledochocholedochostomy? Liver Transpl 2008;14: Tanaka K, Inomata Y, Kaihara S. Living-Donor Liver Transplantation: Surgical Techniques and Innovations. Barcelona, Spain: Prous Science; Haberal M, Sevmis S, Emiroglu R, Karakayali H, Arslan G. Duct-to-duct biliary reconstruction in pediatric liver transplantation: one center s results. Transplant Proc 2007;39: Egawa H, Oike F, Buhler L, Shapiro AM, Minamiguchi S, Haga H, et al. Impact of recipient age on outcome of ABO-incompatible living-donor liver transplantation. Transplantation 2004;77: Weiss S, Schmidt SC, Ulrich F, Pascher A, Schumacher G, Stockmann M, et al. Biliary reconstruction using a side-to-side choledochocholedochostomy with or without T-tube in deceased donor liver transplantation: a prospective randomized trial. Ann Surg 2009;250: Sand J, Airo I, Hiltunen KM, Mattila J, Nordback I. Changes in biliary bacteria after endoscopic cholangiography and sphincterotomy. Am Surg 1992;58: Matthews JB, Gertsch P, Baer HU, Schweizer WP, Blumgart LH. Biliary stricture following hepatic resection. HPB Surg 1991;3:
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