Since the first description of living-donor liver transplantation

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1 CLINICAL AND TRANSLATIONAL RESEARCH Endoscopic Management of Biliary Complications After Adult Living-Donor Versus Deceased-Donor Liver Transplantation Carlos Macías Gómez, 1,4 Jean-Marc Dumonceau, 2 Mariano Marcolongo, 1 Eduardo de Santibañes, 3 Miguel Ciardullo, 3 Juan Pekolj, 3 Martín Palavecino, 3 Adrian Gadano, 3 and Jorge Dávolos 1 Background. Although data about the incidence and management of biliary complications after deceased-donor liver transplantation (DDLT) are well defined, those pertaining to adult living-donor liver transplantation (LDLT) are conflicting. Methods. We retrospectively compared endoscopic retrograde cholangio-pancreatography (ERCP) findings in 30 LDLT vs. 357 DDLT consecutive adult recipients with duct-to-duct biliary reconstruction. LDLT and DDLT recipients were followed up for median durations of 30.5 and 36.0 months after the last ERCP, respectively. Results. Postoperative biliary complications were more frequently identified at ERCP after LDLT versus DDLT (10/30 [33.3%] vs. 34/357 [9.5%]; P 0.001). Complications mainly consisted of anastomotic biliary strictures (10/30 [33.3%] vs. 27/357 [7.6%]; LDLT vs. DDLT recipients, respectively; P 0.001) and biliary leaks (4/30 [13.3%] vs. 6/357 [1.7%]; LDLT vs. DDLT recipients, respectively; P 0.005; some patients had both complications). Stricture dilation was successful in 4/10 (40%) LDLT vs. 27/27 (100%) DDLT recipients (P 0.001), and bile ducts remained patent up to the end of follow-up without further intervention in 2/10 (20.0%) vs. 21/27 (77.8%) patients, respectively (P 0.002). Endoscopic treatment of bile leaks was successful in 3/4 (75.0%) vs. 5/6 (83.3%) LDLT versus DDLT recipients, respectively (NS). Conclusions. Biliary complications were more frequent after LDLT compared with DDLT. Endoscopic treatment of anastomotic biliary strictures was successful in a minority of patients after LDLT, in contrast with DDLT. Most biliary leaks were successfully treated at endoscopy after LDLT or DDLT. Keywords: Liver transplantation, Living donor, Biliary fistula, Endoscopic retrograde cholangio-pancreatography. (Transplantation 2009;88: ) The authors declare no conflict of interest. 1 Gastrointestinal Endoscopy Unit. Gastroenterology Service, Italian Hospital, Buenos Aires, Argentina. 2 Service of Gastroenterology and Hepatology, Geneva University Hospitals, Geneva, Switzerland. 3 Department of Surgery, Liver Transplantation Section, Italian Hospital, Buenos Aires, Argentina. 4 Address correspondence to: Carlos Macías Gómez, M.D., Service of Gastroenterology, Italian Hospital, Gascón 450, C1181ACH Buenos Aires, Argentina. carlos.macias@hospitalitaliano.org.ar Received 27 February Revision requested 25 March Accepted 28 July Copyright 2009 by Lippincott Williams & Wilkins ISSN /09/ DOI: /TP.0b013e3181bb48c2 Since the first description of living-donor liver transplantation (LDLT) in a pediatric patient (1), this operation has gained popularity in adult patients due to the shortage of cadaveric livers (2). Because LDLT was first performed in patients with biliary atresia, restoration of biliary continuity after LDLT has initially been performed using hepaticojejunostomy. More recently, the use of duct-to-duct biliary anastamoses in LDLT has been popularized due to the supposed advantages of this technique (e.g., easier endoscopic access and absence of biliary contamination by digestive content; 3). However, performing duct-to-duct biliary anastamoses in LDLT is one of the most challenging technical aspects of this procedure, due to the small diameter of the intrahepatic bile ducts and the high incidence of aberrant biliary anatomy (4). With an incidence of approximately 30%, biliary complications are the greatest cause of morbidity after LDLT (5). The spectrum of complications includes biliary stones, bile leaks originating from various sites, and biliary strictures. Limited published data have suggested that the incidence of biliary complications is higher after LDLT compared with deceased-donor liver transplantation (DDLT), but data are conflicting (6 9). Also, although endoscopic treatment is accepted as a first-line therapy to treat biliary complications after DDLT (10), limited data are available with regard to LDLT (7 9, 11 13). We, retrospectively, reviewed biliary complications that developed after LDLT versus DDLT in a liver transplantation cohort from a single institution, and compared short- and longterm success of endoscopic treatment in both populations. PATIENTS AND METHODS Consecutive adult patients referred to the Service of Gastroenterology of the Italian Hospital in Buenos Aires between Transplantation Volume 88, Number 11, December 15, 2009

2 2009 Lippincott Williams & Wilkins Gómez et al January 1995 and December 2006 for endoscopic treatment of suspected biliary complications after liver transplantation were included. Referral was at the discretion of the liver transplant team, which comprised hepatologists and liver transplant surgeons; only patients with duct-to-duct biliary reconstruction were referred for endoscopic retrograde cholangio-pancreatography (ERCP), those with biliodigestive anastamoses being referred for percutaneous cholangiography. Between January 1988 and December 2006, 433 liver transplantations were performed in this hospital in 408 adult patients, including 34 LDLT (30 with duct-to-duct anastomosis and four with biliodigestive anastomosis), starting in November 1998 and 399 DDLT (357 with choledocho-choledochostomy and 42 with a biliodigestive anastomosis). The study population, therefore, comprised 357 DDLT recipients and 30 LDLT recipients, of whom 58 (16.2%) and five (16.7%) patients, respectively, received liver transplantation after the introduction of the model for end-stage liver disease (MELD) score as a policy to allocate liver grafts in Argentina (July 2005). All LDLTs were performed by hepatobiliary surgeons with extensive experience in DDLT and pediatric LDLT; right hepatectomy grafts from adult donors were used in all but one case (a left hepatectomy graft was used in the remaining patient), and biliary reconstructions consisted of duct-to-duct anastomoses (with T-tube insertion in a single patient). Data collected prospectively included age, gender, indication for transplantation, type of graft and of biliary reconstruction, details of the endoscopic procedures, potential complications, and their management. Patients gave informed consent for all the procedures; the study complied with the Declaration of Helsinki regarding investigation in humans, and it was approved by the institutional ethics committee. Methods of Treatment If a biliary complication was suspected based on clinical and laboratory data, this was assessed by magnetic resonance cholangiography after exclusion of liver graft rejection and of hepatic artery thrombosis at histopathology and Doppler ultrasonography, respectively. All ERCPs were performed under general anesthesia by experienced therapeutic biliary endoscopists after routine administration of antibiotic prophylaxis. Endoscopic biliary sphincterotomy was performed in all cases and a variety of guidewires (Wilson-Cook Medical, Inc., Winston-Salem, NC; Terumo, Tokyo, Japan; Boston Scientific Co., Boston, MA), measuring 0.018, 0.025, or inch in diameter, were used (usually with a Torque device) for deep biliary cannulation and to secure access to the intrahepatic bile ducts. Bile duct stones or casts detected by cholangiography were extracted during the same session using Dormia baskets or Fogarty-type catheters. Strictures were dilated using 8 or 10 mm in diameter balloon catheters (Hurricane; Boston Scientific Co.), and this was followed by attempted insertion of transpapillary plastic biliary stents (Wilson-Cook Medical) starting in In case of stent insertion, stent removal was scheduled 3 months later and, at the time of repeat ERCP, no stent was inserted and no further endoscopic treatment was recommended if bile leak was resolved or if stricture dilation was judged satisfactory using previously published criteria (14, 15). Otherwise, stenting was repeated and ERCP was planned 3 months later. Definitions Follow-up duration was calculated from the time of last ERCP up to death or to the end of follow-up. Bile leak resolution was defined as the absence of contrast medium leakage during repeat cholangiography at the time of stent retrieval or, if ERCP was not repeated, as clinical and radiological resolution without subsequent biliary procedure required during follow-up. Biliary stricture resolution was defined as the absence of cholestasis (alkaline phosphatases 2 upper limit of normal values) and of intrahepatic bile duct dilation at ultrasonography during follow-up (14, 15). Short-term success was defined (1) for biliary strictures, as successful endoscopic biliary stricture dilation (possibly associated with stent insertion) followed by 50% decrease in serum bilirubin level within 10 days following ERCP and (2) for biliary leaks, as bile leak resolution within 10 days after ERCP. Longterm success was defined according to previous criteria (15), as the absence of both of the following during follow-up: (1) any episode of cholangitis (2) increase in serum alkaline phosphatase associated with biliary stricture dilation judged unsatisfactory at magnetic resonance cholangiography or repeat ERCP. Statistical Analyses Categorical variables were summarized by counts and proportions; continuous variables were summarized by their median value with the ranges under parentheses. Two-tailed Fisher s exact test was used to test differences between categorical variables, and the Wilcoxon rank sum test was used to compare continuous variables. P values less than 0.05 were considered as statistically significant. Analyses were performed with JMP software (version 5.1.2, SAS, Cary, NC). RESULTS Patient referral for ERCP was more frequent after LDLT compared with DDLT (10/30 [33.3%] vs. 34/357 [9.5%]; P 0.001). Demographic characteristics of LDLT and DDLT recipients referred for ERCP were similar (Table 1). The incidence of biliary complications was slightly higher in the most recent period, after the introduction of the MELD score policy to allocate liver grafts compared with before, but the difference was not statistically significant (33/324 [10.2%] vs. 11/63 [17.5%], before vs. after July 2005, respectively; P 0.096). In the 58 patients who received DDLT after the introduction of the MELD score policy, MELD scores were similar in patients who experienced biliary complications or not (median score [range], 25 (19 42) vs. 23 (14 41), respectively; P 0.388). Among 10 LDLT recipients referred for ERCP, seven had a single duct-to-duct biliary anastomosis and three had two duct-to-duct anastomoses (between the recipient s right and left hepatic ducts and the donor s right anterior and posterior sectorial hepatic ducts). All LDLT recipients referred for ERCP had anastomotic strictures (plus bile leaks and stones in 4 and 2 cases, respectively); in the 34 DDLT recipients, main findings at ERCP included anastomotic strictures (n 24), bile leaks (n 3), bile leaks plus anastomotic strictures (n 3), and biliary stones (n 4). Anastomotic strictures in DDLT recipients were associated with biliary stones, casts, or sludge in 11 (41%) cases.

3 Transplantation Volume 88, Number 11, December 15, 2009 TABLE 1. Characteristics of 44 liver transplant recipients referred for ERCP DDLT (n 34) LDLT (n 10) Male gender, n (%) 16 (47) 4 (40) Age (yr) (median, range) 49 (18 67) 59 (43 67) Etiology of liver disease, n (%) Viral hepatitis 12 (35) 4 (40) 1 Autoimmune 10 (29) 4 (40) Alcohol 3 (9) 1 (10) 1 Hemochromatosis 2 (6) 0 1 Cryptogenic 2 (6) 1 (10) Other a 5 (15) Delay LT-referral (mo) 15.5 (0.2 67) 7.5 (1 33) (median, range) Follow-up duration (mo) (median, range) 36 (1 134) 30.5 (2 53) DDLT, deceased-donor liver transplantation; LDLT, living-donor liver transplantation; LT, liver transplantation. a Including idiopathic adulthood ductopenia, intrahepatic arteriovenous fistula, methotrexate-related hepatic insufficiency, congenital hepatic fibrosis, and hepatic artery thrombosis (one each). Biliary Strictures Biliary strictures were more frequently diagnosed at ERCP after LDLT compared with DDLT (10/30 [33.3%] vs. 27/357 [7.6%]; P 0.001). All strictures were located at the anastomotic level (Table 2). Stricture dilation was successful in 4/10 (40%) LDLT vs. 27/27 (100%) DDLT recipients TABLE 2. ERCP for biliary strictures and leaks in 30 DDLT and 10 LDLT recipients: findings, treatment and outcome a DDLT LDLT P Stricture Total Anastomotic location, n (%) 27 (100) 10 (100) 1 Stones, cast or sludge, n (%) 11 (41) 2 (20) Endoscopic treatment No. ERCP (median, range) 2 (1 3) 2 (1 3) Dilation alone, n (%) 9 (33) 2 (20) Dilation plus stenting, n (%) 18 (67) 2 (20) Long-term success, n (%) 21 (78) 2 (20) Leak Total 6 4 Anastomotic location, n (%) 4 (67) 1 (25) Endoscopic treatment No. ERCP (median, range) 2 (2 2) 3 (2 3) Biliary stenting, n (%) 5 (83) 2 (50) Long-term success, n (%) 5 (83) 3 (75) 1 DDLT, deceased-donor liver transplantation; LDLT, living-donor liver transplantation. a Biliary strictures and leaks were both detected in three DDLT recipients and four LDLT recipients. P (P 0.001). In the six LDLT recipients with failed stricture dilation, a guidewire could not be passed through the stricture despite the use of various tricks; the four remaining patients had stricture dilation using a balloon, associated with plastic biliary stenting in two cases (Table 3). Stricture resolution was observed in the two patients who had received balloon dilation plus stenting, and long-term success ensued (liver function tests are normal 41 months after stent removal in one patient and the other one developed liver insufficiency related to relapsing hepatitis C virus infection that eventually leaded to death 17 months after stent removal). The two patients who had only stricture dilation experienced persisting cholestasis, and they were referred for percutaneous biliary drainage (long-term success rate of endoscopic treatment in LDLT recipients, 20%). Globally, 8 (80%) LDLT recipients had failed endoscopic treatment; they were referred for percutaneous stricture dilation (n 6), hepatico-jejunostomy (n 1), or DDLT (n 1). Percutaneous treatment was successful in three of six attempted cases; two of the three patients with failed percutaneous treatment are doing well after hepatico-jejunostomy and DDLT, whereas the remaining patient (the single one who had received a left hepatectomy graft and also had a bile leak) died due to sepsis after failed percutaneous biliary drainage scheduled on an elective basis 2 months after ERCP. In contrast, endoscopic stricture dilation was successful in all of 27 DDLT recipients who had an anastomotic stricture, and this was complemented with plastic biliary stenting in 18 (66.7%) cases. During a median follow-up of 35 (IQR, 10 91) months after the last ERCP, 6 (22.2%) of these 27 patients had a relapsing stricture, including 2 (22.2%) of 9 patients treated with dilation alone and 4 (22.2%) of 18 patients treated with stricture dilation plus plastic biliary stenting. Stricture relapse was diagnosed at a median of 5 months after the last ERCP. Relapsing strictures were successfully treated by hepatico-jejunostomy (n 5) or repeat endoscopic biliary stenting (n 1). Globally, long-term success of endoscopic dilation of anastomotic strictures complicating LDLT and DDLT was achieved in 2/10 (20.0%) and 21/27 (77.8%) patients, respectively (P 0.002). To take into account potential confounding factors related to changes in the endoscopic technique during the study period, results were compared between LDLT and DDLT recipients who had their first endoscopic treatment after March In this subgroup analysis also, long-term success of endoscopic treatment was significantly higher in DDLT versus LDLT recipients (11/13 [85%] vs. 2/10 [20%], respectively; P 0.003). Biliary Leaks Biliary leaks were more frequently diagnosed at ERCP after LDLT compared with DDLT (4/30 [13.3%] vs. 6/357 [1.7%], respectively; P 0.005). After LDLT, leaks were located at the cut surface of the partial liver graft in most cases (Table 2). Endoscopic treatment included biliary sphincterotomy (this was performed in all liver transplant recipients referred for ERCP), plus stone extraction (n 2) or biliary stenting (n 2). Bile leak resolved in 3 (75.0%) LDLT recipients; no bile leak recurrence was detected in these three patients after a follow-up of 29, 40, and 48 months, respectively. The remaining patient was the patient who had received a left

4 2009 Lippincott Williams & Wilkins Gómez et al TABLE 3. Patient (age/sex) Details of endoscopic treatment in LDLT recipients and long-term outcome Anatomical findings a No ERCP Maximum balloon/stent diameter Success of endoscopic treatment Final outcome Leak 67/M Cut surface leak 3 / Yes No leak relapse b 68/F Cut surface leak 3 10 mm/10f Yes No leak relapse 66/M Anastomotic leak 3 8 mm/10f Yes No leak relapse 49/F Cut surface leak 2 / No Death after failed percutaneous treatment Stricture 67/M Fork shaped 3 / No Percutaneous treatment b 55/F Crane neck 2 8 mm/ No Percutaneous treatment 49/F Pouched type 1 8 mm/ No Liver retransplantation 68/F Fork shaped 3 10 mm/10f Yes No relapse 56/F Crane neck 2 / No Hepatico-jejunostomy 43/M Pouched type 1 / No Liver retransplantation 64/M Crane neck 2 / No Hepatico-jejunostomy 66/M Unbranched 3 8 mm/10f Yes No relapse 70/F Multibranched 1 / No Percutaneous treatment 49/F Multibranched 2 / No Death after failed percutaneous treatment LDLT, living-donor liver transplantation; NA, not applicable. a Stricture anatomy was defined according to Hisatsune et al. (13), Yoshimoto et al. (22), and Kim et al. (21). b This patient eventually underwent percutaneous treatment because the stricture could not be traversed despite repeated endoscopic attempts, although bile leak had resolved after biliary sphincterotomy. FIGURE 1. (A) Anastomotic biliary stricture (unbranched shape) after living-donor liver transplantation; (B) guidewire passed through the stricture; (C) stricture dilation using a 10-mm in-diameter balloon; and (D) 10F plastic biliary stent.

5 Transplantation Volume 88, Number 11, December 15, 2009 hepatectomy graft and who died after failed percutaneous biliary drainage. In DDLT recipients, endoscopic biliary sphincterotomy plus stenting was performed in five of six cases, and this was always followed by bile leak resolution. The remaining patient had a complete bile duct disruption, and he was referred for hepatico-jejunostomy. Treatment Complications Post-ERCP complications developed in 1 (10.0%) LDLT recipient (cholangitis successfully treated by temporary percutaneous transhepatic biliary drainage) and 3 (8.8%) DDLT recipients (one mild pancreatitis and two cholangitis that resolved with medical treatment). DISCUSSION ERCP referral for biliary complications was significantly more frequent after LDLT compared with DDLT (33.3% vs. 9.5%, P 0.001). This corroborates the results of two other series (totaling 275 and 180 patients) that reported biliary complications more frequently after LDLT compared with DDLT (73% vs. 25% [P 0.001] and 26% vs. 7% [P 0.004], respectively; 7, 16). However, a larger series (n 429) has reported identically low incidences of biliary complications (5.8%) after LDLT or DDLT (6). In one of the series cited above (7), bile leaks were extremely frequent (53%) suggesting that a technical factor might have contributed to a significant proportion of these complications. Indeed, some technical factors (namely, an interrupted rather than a continuous suture and performance of multiple biliary anastomoses) are known to favor the development of biliary complications after LDLT (17, 18). Surgical expertise has also likely contributed to the exceptionally low incidence of biliary complications after LDLT reported by Park et al. (5.8%; 6), although the role of other factors in this series (e.g., biliary complications had to be confirmed by endoscopic or percutaneous cholangiography to fulfill definition criteria, type of anastomosis [not stated]) cannot be excluded. This high incidence of biliary complications after LDLT compared with DDLT has lead to a significant reduction in the number of LDLT in many centers. Duct-to-duct biliary reconstruction is favored over hepatico-jejunostomy for LDLT in many centers (as it is for DDLT) to prevent ascending cholangitis and to facilitate endoscopic access to the bile ducts (3). However, in our experience, the endoscopic treatment of biliary complications (in particular that of anastomotic stenosis) was disappointing after LDLT, whereas it yielded results in LDLT recipients that were as good as those reported by other authors (14, 19, 20). Five other series including at least 10 patients have reported the results of endoscopic treatment for anastomotic biliary strictures (Figs. 1 and 2) complicating LDLT, and short-term success rates were higher compared with our series (63% 71% vs. 40%) (8, 11 13, 21). This difference in success rates may, in our opinion, be attributed to anatomical findings. Crane-neck deformity and a pouched shape (Fig. 3) of the distal part of the anastomosis after LDLT have been described FIGURE 2. (A) Anastomotic biliary stricture (fork shaped) and upstream sludge after living-donor liver transplantation; (B) stricture dilation using a 10-mm in-diameter balloon; (C) 10F plastic biliary stent; and (D) absence of residual stricture at late follow-up. FIGURE 3. Failed endoscopic treatment in three patients with anastomotic biliary stricture after living-donor liver transplantation. (A) multibranched stricture; (B) pouched shape stricture; and (C) Crane-neck deformity, with the common bile duct severely bent (occlusion cholangiography with guidewire below the stricture).

6 2009 Lippincott Williams & Wilkins Gómez et al as ERCP findings that were associated with significantly lower success rates of endoscopic treatment (20% and 25%, respectively) compared with other anatomical presentations (21, 22). The proportion of LDLT recipients with a crane-neck deformity in our series was exceptionally high (30% vs. 7% in another large series; 22), and this has likely contributed to our low success rate. Another difficulty reported by other authors in LDLT recipients that we also frequently encountered was an inadequate positioning of the endoscope, not in front of the papilla (the duodenoscope was sharply bent in the antrum, due to compression by the liver graft) (13). Finally, bile leaks in our LDLT recipients were most frequently located at the level of the cut surface of liver grafts, in contrast with previous studies that reported leaks at the anastomosis level in more than 80% of cases (7, 8). The low incidence of anastomotic leaks in our patients is possibly related to the absence of external stent tube in our patients: external stent tubes have been shown in a randomized trial to be associated with an increased incidence of biliary complications in DDLT, including biliary leakage after tube removal, but their use in LDLT is controversial (3, 18). As for cutsurface leaks, their incidence is in keeping with reports from other series, and it can be reduced by experience, with meticulous attention in the section plane, and testing with injection of preservation solution during preparation of the graft on the backtable. With regard to the endoscopic treatment of bile leaks after LDLT, our success rate was similar to those reported in other series (the single patient with unsuccessful endoscopic treatment had a leak-located upstream from a tight stricture; 7, 8, 11, 12). In summary, biliary complications were significantly more frequent after LDLT compared with DDLT, and they were less amenable to endoscopic treatment. Endoscopic treatment was successful in a minority of LDLT recipients only, in contrast with the good results in DDLT recipients. The low success rate of endoscopic treatment in LDLT recipients was likely attributable to biliary anatomy, that is challenging to the endoscopist. REFERENCES 1. Strong RW, Lynch SV, Ong TH, et al. Successful liver transplantation from a living donor to her son. N Engl J Med 1990; 322: Brown RS, Russo MW, Lai M, et al. A survey of liver transplantation from living adult donors in the United States. N Engl J Med 2003; 348: Dulundu E, Sugawara Y, Sano K, et al. Duct-to-duct biliary reconstruction in adult living-donor liver transplantation. Transplantation 2004; 78: Kim RD, Sakamoto S, Haider MA, et al. Role of magnetic resonance cholangiography in assessing biliary anatomy in right lobe living donors. 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