Efficacy of endoscopic and percutaneous treatments for biliary complications after cadaveric and living donor liver transplantation

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1 Efficacy of endoscopic and percutaneous treatments for biliary complications after cadaveric and living donor liver transplantation Ju Sang Park, MD, Myung-Hwan Kim, MD, Sung Koo Lee, MD, Dong Wan Seo, MD, Sang Soo Lee, MD, Jimin Han, MD, Young Il Min, MD, Shin Hwang, MD, Kwang Min Park, MD, Young Joo Lee, MD, Seung Gyu Lee, MD, Kyu Bo Sung, MD Seoul, Korea Background: Percutaneous transhepatic radiologic procedures as well as ERCP-based techniques have been used to treat biliary complications after liver transplantation. However, the efficacy of these treatments has not yet been clarified, especially for complications occurring after living donor liver transplantation. Methods: A retrospective study was performed to determine the frequency and types of the biliary complications after cadaveric donor liver transplantation and living donor liver transplantation. The success of ERCP and percutaneous transhepatic radiologic procedures was also evaluated. The choice of treatment approach, ERCP or percutaneous transhepatic radiologic procedures, depended on the type of biliary reconstruction and accessibility of the lesion. Results: Among 429 adult patients who underwent liver transplantation, 39 biliary complications developed in 25 patients (5.8%): biliary stricture (20), biliary stones (10), and bile leak (9). The frequency of biliary complications (5.8%; 6/103) after cadaveric donor liver transplantation was not significantly different compared with that after living donor liver transplantation (5.8%; 19/326). Success rates for treatment of biliary complications by means of ERCP and percutaneous transhepatic radiologic procedures were, respectively, 100% (11/11) and 78% (18/23). For endoscopically treated patients, balloon dilation alone for biliary strictures and nasobiliary tube placement alone for bile leaks resulted in complete resolution of the complication in, respectively, 67% (2/3) and 40% (2/5) without further intervention. Conclusions: Transpapillary endoscopic and percutaneous transhepatic radiologic interventions are both effective therapies for biliary complications associated with liver transplantation. They are complementary approaches that help to avoid surgery for these complications. (Gastrointest Endosc 2003;57:78-85.) Although surgical techniques, methods of graft preservation, and immunosuppressive drugs for liver transplantation have steadily improved, biliary complications continue to be a significant cause of morbidity and mortality in patients undergoing liver transplantation and a significant influence on graft survival. 1-3 Biliary complications reportedly occur after 6% to 34% of cadaveric donor liver transplantation (CDLT). 1-7 Early diagnosis and prompt adequate treatment of biliary complications are, therefore, indispensable to reducing morbidity and mortality related to liver transplantation. 4 Received December 17, For revision March 8, Accepted September 25, Department of Internal Medicine, General Surgery, and Interventional Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea. Reprint requests: Myung-Hwan Kim, MD, Department of Internal Medicine, Asan Medical Center, 388-1, Pungnapdong, Songpagu, Seoul, , Korea. Copyright 2003 by the American Society for Gastrointestinal Endoscopy /2003/$ doi: /mge Living donor liver transplantation (LDLT) is being performed increasingly, especially in Eastern Asian countries including Korea and Japan, because of the limited availability of cadaver donors. LDLT has already become a standard therapy for pediatric recipients and is also gaining acceptance for adults. 5,8-12 A precise rate for biliary complications after LDLT in adults, however, has not been reported. Traditionally, surgical repair has been the primary approach to management of biliary complications after liver transplantation. 7,8 Although therapeutic endoscopic and interventional radiologic techniques have now replaced surgery to a certain degree, 1,3,7,13-24 the efficacy of these treatments has not been precisely clarified. This retrospective study was conducted to determine the frequency and type of biliary complications after CDLT and LDLT. The therapeutic role of transpapillary endoscopic and percutaneous transhepatic radiologic procedures (PTRP) for the various biliary complications after CDLT and LDLT were also evaluated. 78 GASTROINTESTINAL ENDOSCOPY VOLUME 57, NO. 1, 2003

2 A C PATIENTS AND METHODS A total of 429 adult patients (age range years) underwent liver transplantation (103 CDLT, 326 LDLT) at our medical center from January 1992 to June Biliary reconstruction was by choledochocholedochostomy (C-C) or hepaticojejunostomy (H-J) as determined by multiple factors including the underlying liver disease, relative sizes of donor and recipient bile ducts, and prior biliary surgery. A biliary complication was diagnosed in 25 patients (5.8%; 18 men, 7 women; mean age 47 years, range, years). These patients constituted the study group. The indication for transplantation, donor type, and method of biliary reconstruction are presented in Table 1. The diagnosis of biliary complications was based on clinical symptoms, laboratory tests, and imaging studies including transabdominal US, CT, diisopropyl iminodiacetic acid (DISIDA) scan, ERCP, and/or percutaneous transhepatic cholangiography (PTC). Median follow-up from transplantation to last follow-up was 20 months (range, 4-53 months). B Figure 1. A, Retrograde cholangiogram showing biliary stricture (large arrow) at anastomotic site and bile duct stones (small arrow) distal to stricture. B, Retrograde cholangiogram after stone removal with balloon (small arrow) showing significant biliary stricture (large arrow). C, Retrograde cholangiogram made by means of nasobiliary tube 2 days after balloon dilation showing persistent stricture (arrow).a plastic stent was placed across stricture. Table 1. Characteristics of patients with biliary complications Indication for liver transplantation, n (%) End-stage liver disease 20/25 (80) Hepatoma 4/25 (16)* Fulminant hepatitis 1/25 (4) Type of donor CDLT 6/25 (24) LDLT 18/25 (72) Both 1/25 (4) Type of biliary reconstruction C-C 14/25 (54)* H-J 12/25 (46)* CDLT, Cadaver donor liver transplantation; LDLT, living donor liver transplantation; C-C, choledochocholedochostomy; H- J, hepaticojejunostomy. *One patient underwent both types of biliary reconstruction. Diagnosis of biliary complications After liver transplantation, recipients underwent laboratory tests, Doppler US, and conventional radiographic imaging studies on a routine basis and whenever significant clinical symptoms developed including fever, abdominal pain, jaundice, or new-onset ascites. The presence of a biliary stricture, as suggested by an obstructive pattern of liver function tests, bile duct dilatation on US and CT, and intraductal stasis of radiolabeled hepatobiliary agent on DISIDA scan, was confirmed by either ERCP or PTC. A significant biliary stricture was defined as an abrupt luminal narrowing with proximal ductal dilatation. The VOLUME 57, NO. 1, 2003 GASTROINTESTINAL ENDOSCOPY 79

3 A C presence of a biliary stone, as suggested by echogenic intraductal material with acoustic shadowing on US and/or intraductal hyperdense material on pre-enhanced abdominal CT, with or without proximal bile duct dilatation, was confirmed by ERCP or PTC. Bile leak was confirmed by DISIDA scan and demonstration of leakage of contrast medium from the duct at ERCP or PTC. Treatment modalities A transpapillary or percutaneous transhepatic approach was selected for treatment of a biliary complication depending on accessibility of the lesion and the type of biliary reconstruction. As a general rule, transpapillary intervention was chosen for lesions located distal to the left and right main hepatic ducts, whereas the percutaneous approach was selected for lesions proximal to these ducts. Also, the former approach was used in patients with a C-C reconstruction and the latter for those with a H-J. However, the percutaneous approach was used in patients with a C- B Figure 2. A, Retrograde cholangiogram showing contrast leakage (arrow) from site of T-tube removal. B, Retrograde cholangiogram 2 weeks after endoscopic sphincterotomy and nasobiliary tube drainage showing persistent leakage of contrast (arrow). A plastic stent was placed. C, Retrograde cholangiogram 2 months after stent removal showing no further leakage of contrast from leak site (arrow). C when an initial approach by means of ERCP was unsuccessful or the general condition of the patient precluded ERCP. When endoscopic and/or percutaneous treatment both failed, surgery was performed such as retransplantation or reconstruction of the bile duct depending on the medical condition of the patient. Informed consent was obtained for all procedures from all patients. Transpapillary endoscopic intervention Biliary strictures were dilated with 8- to 10-mm diameter balloons followed by placement of a 5F nasobiliary tube across the stricture. If the stricture was not evident on follow-up cholangiograms made through the nasobiliary tube, treatment was considered to be completed. If a stricture was evident on follow-up cholangiogram, a 10F single plastic stent was placed (Fig. 1). Biliary stones were removed by using a basket and/or a standard retrieval balloon after endoscopic sphincterotomy (EST). Bile leak was treated by EST followed placement of a 5F nasobiliary tube placement across the leak site. When the leak was no longer evident on follow-up nasobiliary tube cholangiography, treatment was considered completed. If the bile leak was persistent on follow-up cholangiography, a 10F plastic stent was placed across the leak site (Fig. 2). Percutaneous transhepatic radiologic intervention Biliary strictures were dilated with 6- to 8-mm diameter balloons followed by placement of a 10F drainage catheter across the stricture by means of the percutaneous transhe- 80 GASTROINTESTINAL ENDOSCOPY VOLUME 57, NO. 1, 2003

4 A B C Figure 3. A, Cholangiogram made by PTBD tube showing multiple intrahepatic duct stones (small arrows) and long biliary stricture (arrowheads) at hepaticojejunostomy. A portal vein stricture was treated by insertion of a metal stent (large arrow). B, Cholangiogram made after stone removal from posterior intrahepatic duct. Stones are being removed from anterior intrahepatic duct with basket (small arrow) by means of a new PTBD tract (large arrow) because acute angulation between anterior and posterior intrahepatic ducts precluded an approach to anterior duct through posterior duct. C, Cholangiogram showing balloon dilation (arrow) of anastomotic stricture at hepaticojejunostomy. D, Cholangiogram made 1 month later showing clearance of stones and resolution of anastomotic stricture (arrowheads). D patic biliary drainage (PTBD) tract. If the stricture was not resolved on follow-up cholangiography, the catheter was exchanged for a 12F to 14F catheter. If the stricture was resolved on follow-up cholangiography, the catheter was withdrawn until the tip was located just proximal to the initial stricture site. If the stricture was still resolved on subsequent cholangiography, the catheter was removed. When recurrence of the stricture was demonstrated on follow-up cholangiography, the catheter was reinserted across the stricture after balloon dilation (Fig. 3). Biliary stones were removed with a basket through the PTBD tract without prior dilation. Bile leak was treated by placement of PTBD catheter by means of the percutaneous tract, the catheter being maintained across the leak site until the leak resolved. Definition and analysis of successful treatment Successful treatment of the biliary complication was defined as follows: (1) complete resolutions of clinical symptoms, laboratory test abnormalities, and abnormal imaging findings (e.g., US or CT); (2) direct cholangiographic demonstration of resolution of the complication at completion of treatment; (3) no recurrence of clinical symptoms and/or signs of the complication after treatment (e.g., after removal of a stent or tube placed for the treatment); and (4) absence of evidence of the biliary complication on follow-up cholangiography. Cases in which treatment was ongoing (e.g., endoscopic stent of PTBD catheter still in place) or death occurred from causes unrelated to the biliary complication were excluded from the VOLUME 57, NO. 1, 2003 GASTROINTESTINAL ENDOSCOPY 81

5 Table 2. Frequency of occurrence and type of biliary complications Frequency of biliary complications Patients/total, n (%) 25/429 (5.8) Cases 39* According to donor CDLT 6/103 (5.8) LDLT 19/326 (5.8) Types of biliary complications, n (%) Biliary stricture 20/39 (51) Biliary stone 10/39 (26) Bile leak 9/39 (23) CDLT, Cadaver donor liver transplantation; LDLT, living donor liver transplantation. *Fourteen patients had multiple complications. Table 3. Frequency of occurrence of each biliary complication according to donor type Biliary Biliary Bile Type of stricture stone leak donor, n (%) (n = 20) (n = 10) (n = 9) CDLT (n = 103) 4/103 (3.9)* 3/103 (2.9) 2/103 (1.9) LDLT (n = 326) 16/326 (4.9) * 7/326 (2.1) 7/326 (2.1) CDLT, Cadaver donor liver transplantation; LDLT, living donor liver transplantation. *p = in comparison of biliary stricture between type of donor. p = in comparison of biliary stone between type of donor. p = in comparison of bile leak between type of donor. analysis of the results of endoscopic and percutaneous therapy. All statistical analyses were performed with statistical software (SPSS 10.0, SPSS, Inc., Chicago, Ill.) statistical software program. Categorical and continuous variables were compared with the chi-square test, the Fisher exact test, and the Student t test. The log rank test was used to compare the Kaplan-Meier curves for the occurrence of each biliary complication according to the type of bile duct reconstruction. A p value of < 0.05 was considered statistically significant. RESULTS Frequency and type of biliary complications Biliary complications developed in 25 (5.8%) of 429 patients undergoing liver transplantation; these occurred in 6 (5.8%) of 103 who underwent CDLT and 19 (5.8%) of 326 who had LDLT. There were 39 complications in total; 14 patients had 2 complications. Biliary complication included stricture (n = 20), stone(s) (n = 10), and leak (n = 9) (Table 2). Stricture, stone, and leak occurred, respectively, in 3.9% (4/103), 2.9% (3/103), and 1.9% (2/103) of patients who underwent CDLT, and 4.9% (16/326), 2.1% (7/326), and 2.1% (7/326), respectively, who had LDLT. No difference was found between CDLT and Table 4. Proportion of biliary complications according to type of bile duct reconstruction and site Biliary Biliary Bile stricture stone leak (n = 20) (n = 10) (n = 9) Type of reconstruction, n (%) C-C (n = 18) 8/20 (40) 4/10 (40) 6/9 (67) H-J (n = 21) 12/20 (60) 6/10 (60) 3/9 (33) Type of site Anastomosis 18/20 (90) 9/10 (90) 4/9 (44) Non-anastomosis 2/20 (10) 1/10 (10) 0 (0) T-tube removal 0 (0) 0 (0) 4/9 (44) Resection margin 0 (0) 0 (0) 1/9 (11) C-C, Choledochocholedochostomy; H-J, hepaticojejunostomy. LDLT when the frequency of occurrence and type of biliary complication were compared (80% power to detect a difference of 10%; Table 3). The proportions of patients with stricture, stone, and leak among those who had a C-C reconstruction were, respectively, 40% (8/20), 60% (12/20), and 40% (4/10); among patients with a H-J, the respective proportions were 60% (6/10), 67% (6/9), and 33% (3/9) (Table 4). There was no statistically significant difference between these 2 patient groupings with respect to frequencies of each type of complication (Fig. 4). Biliary stricture The median (interquartile range [IQR]) time interval between onset of the biliary stricture and liver transplantation was 5.9 months ( ). The stricture involved the anastomotic site in 18 (90%) of the 20 patients with this complication (Table 4). Five patients (25%) underwent ERCP and 15 (75%) PTRP. Therapy by means of ERCP was successful in 2 patients with EST and balloon dilation alone, whereas the other 3 required insertion of a plastic stent. Of the 3 patients in whom a stent was placed, 2 were excluded from the analysis of success; in one treatment was ongoing and the other died from reactivation of hepatitis during treatment. Thus, only 1 patient was successfully treated with stent placement. Of the 15 patients who underwent PTRP, 9 were successfully treated with balloon dilation of the stricture and placement of a catheter across the site. Of 3 patients in whom PTRP was unsuccessful, 1 ultimately underwent H-J because a severe stricture at the anastomosis led to complete isolation of the right anterior duct; biliary reconstruction was successful. The other 2 patients underwent retransplantation because the severe stricture eventually led to severe secondary biliary cirrhosis and graft dysfunction; both died of acute respiratory distress syndrome and sepsis after transplantation. Of the 82 GASTROINTESTINAL ENDOSCOPY VOLUME 57, NO. 1, 2003

6 Table 5. Success of therapeutic procedures Total Biliary Biliary Bile complication stricture stone leak Success rate (n = 34)* (n = 15)* (n = 10) (n = 9) Overall, n (%) 29/34 (85) 12/15 (80) 9/10 (90) 8/9 (89) ERCP 11/11 (100) 3/3 (100) 3/3 (100) 5/5 (100) PTRP 18/23 (78) 9/12 (75) 6/7 (86) 3/4 (75) *Five of 39 cases were excluded in this analysis because of ongoing treatment. 15 patients who underwent PTRP, 3 were excluded from the analysis because of death due to rejection and hepatitis reactivation during treatment. The ERCP and PTRP approaches were successful in treating biliary stricture in, respectively, 100% and 75% of cases (Table 5). Biliary stone The median (IQR) time interval between development of biliary stone and liver transplantation was 11.8 months ( ). In 9 (90%) of the 10 patients with this complication the stone was at the anastomotic site (Table 4). Nine patients had an associated biliary stricture and 1 a leak. Three patients underwent ERCP and 7 PTRP. In the former group, all biliary stones were removed at a single ERCP. Of the 7 patients who underwent PTRP, the treatment was successful in 6; the seventh patient ultimately underwent retransplantation because of severe, intractable obstruction of the bile duct caused by the stone and accompanying stricture, which led to graft dysfunction. This patient died as a result of acute respiratory distress syndrome after transplantation. ERCP and PTRP were successful in managing biliary stones in, respectively, 100% and 86% of cases (Table 5). Bile leak The median (IQR) time interval between development of bile leak and liver transplantation was 0.7 months ( ). Of the 9 patients with this complication, the leak was located at the anastomosis in 4 (44%), the site of removal of a T-tube in 4 (44%), and the resection margin in 1 (11%) (Table 4). Five patients (56%) underwent ERCP and 4 (44%) PTRP. Of the 5 who underwent ERCP, 2 were successfully treated with EST and nasobiliary tube insertion alone whereas the other 3 required additional plastic stent insertion across the leak site. Three of the 4 patients who underwent PTRP were successfully treated by keeping the tube across the leak site. One patient did not respond to the PTRP and ultimately underwent retransplantation because of transformation of a biloma into an A B C Figure 4. Kaplan-Meier curves showing occurrence rates of biliary complications in relation to type of bile duct reconstruction. A, Biliary stricture; B, biliary stone; C, bile leak. C- C, Choledochocholedochostomy; H-J, hepaticojejunostomy. VOLUME 57, NO. 1, 2003 GASTROINTESTINAL ENDOSCOPY 83

7 abscess with progression to septic shock. The patient was treated successfully by retransplantation. The success rates for ERCP and PTRP in treating bile leak were, respectively, 100% and 75% (Table 5). Complication of ERCP and PTRP ERCP- and PTRP-related complication rates were, respectively, 23% (3/13) and 15% (4/26). Mild post-ercp pancreatitis developed in two patients who underwent ERCP for bile leak, but it resolved spontaneously. One patient who underwent endoscopic insertion of a biliary stent for bile leak had acute cholangitis develop because of early clogging of the stent. Stent removal and insertion of an endobiliary tube resulted in clinical improvement. Hemobilia and cholangitis developed in three patients who underwent PTBD before PTRP. In 2, these complications resolved spontaneously with conservative treatment; the other was managed by coil embolization for a pseudoaneurysm of the right hepatic artery. A hemothorax developed in one patient who underwent PTBD; the hematoma was evacuated by video-assisted thoracoscopic surgery. DISCUSSION The overall frequency of biliary complications (5.8%, 25/429) after liver transplantation in the present study was lower than that (6%-34%) of previous studies. 2 Biliary complications developed in 19 (5.8%) of 326 patients who underwent LDLT and 6 (5.8%) of 103 who had CDLT. To date, the reported frequency of biliary complications in patients who underwent LDLT has been 18% to 39% in 3 English language reports of series that mainly included pediatric patients. 8,9,11 Cronin et al. 8 found that the frequency (39%) of biliary complications in pediatric patients undergoing LDLT was higher than that (14%) for patients who had CDLT. By comparison, the results of the present study indicate that the frequency of biliary complications in adults who undergo LDLT is the same as that for patients who have CDLT (Table 2). Nine of the 10 patients with biliary stones in the present study also had biliary strictures, suggesting that stricture formation plays an important role in stone development. Most stones were located proximal to the stricture. However, 3 of the 10 patients had stones distal to anastomotic strictures (Fig. 1). This may be due to postoperative denervation of the sphincter of Oddi and subsequent sphincter dysfunction after liver transplantation. 25,26 Dysfunction may alter bile flow into the duodenum, which may eventually induce stone formation. Several studies have suggested that balloon dilation alone might be unreliable therapy for anasto- motic strictures after CDLT, and the investigators recommended that balloon dilation be followed by stent placement for a more durable result. 17,19 In the present study, 67% of patients who underwent ERCP were successfully treated with only EST and balloon dilation of the stricture. Morelli et al. 27 studied endoscopic treatment of post-transplantation bile leaks and suggested that placement of a leakbridging stent was safe and effective. In the present study, 2 of 5 patients with bile leaks and a C-C reconstruction were successfully treated with only EST and temporary insertion of a nasobiliary tube. Based on our experience with the treatment of biliary stricture and bile leak, the additional endoscopic placement of a stent was not always necessary in the former case if dilation was easily accomplished at a single session, and in the latter case if effective drainage of bile was accomplished by placement of a nasobiliary tube. Although patients tend to prefer a plastic stent to a nasobiliary tube because of the inconvenience associated with the latter, the nasobiliary tube has several advantages. First, and most important, ERCP is not required for removal of the nasobiliary tube. Second, follow-up cholangiography is much easier and bile samples can be obtained for culture by using the nasobiliary tube. Third, occlusion of the nasobiliary tube is readily recognized when there is a decrease in the volume of bile drainage and can be prevented by frequent irrigation with saline solution. It has been suggested that PTRP, including balloon dilation and/or placement of a metal stent, can be highly useful for ameliorating post-transplantation biliary strictures. 11,12,22,23 However, 9 of the 12 patients with biliary stricture in the present study who underwent PTRP were successfully treated by balloon dilation and maintenance of drainage by placement of a tube across the stricture. Metal stents were not used because long-term results with this device in the management of biliary strictures with respect to patency are poor and stent removal is difficult. 28 The success rates in the present study for ERCP and PTRP in the treatment of biliary complications were, respectively, 100% (11/11) and 78% (18/23) (Table 5). However, this simple comparison is misleading and must be interpreted with caution because the choice of treatment modality mainly depended on the type of biliary reconstruction and access to the complication site. Moreover, the number of patients in each group was relatively small. Because the study design was retrospective, interpretation is also limited with respect to the potential for complications in relation to types of liver transplantation and biliary reconstruction. Transpapillary 84 GASTROINTESTINAL ENDOSCOPY VOLUME 57, NO. 1, 2003

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