Laparoscopic cholecystectomy (LC) is the treatment

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1 Management and Outcome of Major Bile Duct Injuries After Laparoscopic Cholecystectomy: From Therapeutic Endoscopy to Liver Transplantation Arno Nordin, Leena Halme, Heikki Mäkisalo, Helena Isoniemi, and Krister Höckerstedt Laparoscopic cholecystectomy is associated with a higher rate of bile duct injuries than an open cholecystectomy. The annual incidence of bile duct injuries has remained almost constant and these injuries tend to be more serious, making demands on the method of repair. We wanted to report the management and outcome of major bile duct injuries after laparoscopic cholecystectomy in patients referred to a hepatobiliary and liver transplantation unit. Eighteen patients (14 women), with a median age of 53.5 years were referred to the liver surgery unit with a major bile duct injury after laparoscopic cholecystectomy. The injury was identified after a median of 3 days (range, 0 to 25 days) after operation and the median time interval to referral was 79 days (0 to 2270 days). Fourteen patients had undergone surgery before referral. By the time of referral, four patients had developed end-stage cirrhosis, necessitating liver transplantation. Three of them had undergone bilioenteric drainage operations at the referring institute. Of the remaining 14 patients, three were managed by therapeutic endoscopic procedures. Ten patients were managed with Roux-en-Y hepaticojejunostomy. One died of septic complications before the repair. A median time for hospitalization in our unit was 33 days (range,10 to 164 days). At present, 16 patients are alive. One patient died of Kaposi s sarcoma 7 months after liver transplantation. A long interval between bile duct injury and referral was associated with the development of endstage liver disease. Surgery of biliary lesions is demanding, and surgical experience with multidisciplinary approach, including therapeutic endoscopy and liver transplantation, is necessary for successful outcome. (Liver Transpl 2002;8: ) From the Transplantation and Liver Surgery Unit, Helsinki University Hospital, Helsinki, Finland. Address reprint requests to Arno Nordin, MD, Transplantation and Liver Surgery Unit, Helsinki University Hospital, PO Box 263, FIN HUS, Helsinki, Finland. Telephone: ; FAX ; arno.nordin@hus.fi Copyright 2002 by the American Association for the Study of Liver Diseases /02/ $35.00/0 doi: /jlts Laparoscopic cholecystectomy (LC) is the treatment of choice for symptomatic cholecystolithiasis. Laparoscopic approach is associated with a higher rate of major bile duct injuries compared with open cholecystectomy. The incidence of bile duct injury has remained quite stable between 0.33% and 0.5% throughout the early periods of LC 1,2 into the present. 3-6 Bile duct injuries related to LC seem to be more complicated than after an open procedure. 7-9 On many occasions, subsequent treatments have failed in the primary hospital, leading to a sequence of reoperations and various interventions. The delay in the definitive treatment and the high number of interventions before referral may increase the cost of the management and patient morbidity. 7,10-13 Surgeons performing laparoscopic surgery should be aware of the possibility of a major complication and how to handle it. We present a series of patients with major bile duct injury to improve the knowledge of the complicated nature of these lesions and to stress the possibility of the ultimate consequence, namely liver transplantation. Patients and Methods Patients referred to the liver unit for major bile duct injury sustained during LC were evaluated retrospectively. The information regarding primary operative procedure, presenting symptoms, the type and level of biliary tract injury, diagnostic procedures, and therapeutic interventions before and after referral was obtained from patient records. The diagnostic methods to detect the level and extent of the bile duct injury as well as complications caused to other organs, the liver in particular, included endoscopic retrograde cholangiography (ERC), percutaneous transhepatic cholangiography (PTC), ultrasound examination, computed tomography and magnetic resonance imaging, liver function tests, and laparotomy. The injuries were classified according to the system introduced by Strasberg et al. 8 Injury types A, B, C, and D (i.e., bile leak or a lesion in an aberrant duct, leak from cystic duct stump or a lateral lesion in the common bile duct, respectively) were excluded from the study. All patients had a severe injury, type E, in which the continuity between the biliary tree and the intestine is lost. This separation may be caused by a stenosis of the duct, complete occlusion of the bile duct, or loss of ductal tissue. Type E lesions are divided further into subtypes according to Bismuth. 14 The first four subtypes refer to the upper level of the lesion. In type E1, the lesion is more than 2 cm below the hepatic bifurcation; in E2, this distance 1036 Liver Transplantation, Vol 8, No 11 (November), 2002: pp

2 Management of Major Iatrogenic Bile Duct Injuries 1037 Table 1. Patient Characteristics, Day of Recognition of the Injury Postoperatively, Initial Treatment, and Time Interval Between the Date of Injury Recognition and the Date of Referral Patient Age (yr) Gender Injury Noted at Day Treatment Before Referral Time Interval (d) 1 54 F 6 Laparotomy, clip removal, T-tube F 2 Laparotomy, suture repair, T-tube; ERC F 0 Suture repair T-tube F 10 HJS T-tube F 18 None M 8 Laparosc, drainage; HJS F 18 PTC drainage F 0 Suture repair T-tube; dilatations F 2 None F 0 Suture repair, external drainage M 3 Laparotomy, external drainage F 0 CDS; relaparotomy canalisation F 20 Laparotomy, external drainage F 5 Laparotomy, external drainage M? None 1, F 0 HJS T-tube; PTC dilatations 2, F 0 HJS; re-hjs 2, CJS Hepp-Couinaud 2, M 3 HJS; JS endosc dilatations 1,196 Abbreviations: ERC, Endoscopic retrograde cholangiography; HJS, hepaticojejunostomy; PTC, percutaneous transhepatic cholangiography; CDS, choledochoduodenostomy; CJS Hepp-Couinaud, cholangiojejunostomy by the method of Hepp-Couinaud into the left biliary duct; JS, jejunocutaneostomy. is less than 2 cm; in E3, the lesion is at the bifurcation but the continuity between lobar bile ducts is not lost; and in type E4, the lesion extends into one or both of the intralobar ducts. Type E5 is a combined common hepatic and aberrant right duct injury. The injury was classified before the definitive treatment. The final therapy was based on therapeutic endoscopy, radiologically guided interventions, and surgery (hepaticojejunostomy [HJS] and liver transplantation). Establishment of biliary drainage and treatment of sepsis preceded definitive repair. A period of 3 months was allowed for the inflammation to subside and ischemia of the bile ducts to reach a final level. Surgical approach was by a right subcostal incision extended slightly to the opposite side. The dissection of the biliary tree was carried cranially along the anterior side of the ductal plate to obtain viable bile duct with well-vascularized epithelium. The exposed bile ducts were divided, and no further dissection above that level was performed to avoid damage in periductal tissue. The base of segments 4B or 5 was cored, if necessary. The actual anastomosis was carried out with interrupted 5-0 absorbable (polydioxanon) sutures into Roux-en-Y jejunal loop at least 45 cm long. The posterior row of sutures was tied intraluminally. In a majority of cases, the dissection had to be carried above the bifurcation, resulting in two or three open bile ducts. In such cases, the anastomoses were performed separately. Intraluminal stents were not used. The patients were followed up in outpatient clinic. The information of their condition was obtained from patient records or, if not available, by telephone interview with the patients. Patients who underwent liver transplantation were followed according to protocol. Results Presentation and Management Before Referral Primary LC. A total of 18 patients from 11 different hospitals were referred to the liver unit between 1992 and In two patients (11%), the indication for primary operation was acute cholecystitis, in the others symptomatic cholelithiasis. Male-to-female ratio was 4:14. The median age was 53.5 (range, 20 to 71) years at referral. The patient demographics, the therapy before and after referral, and the time period between injury recognition and referral are shown in Tables 1 and 2. The primary operation was described as uneventful in five patients (28%). The most frequent complaint of the surgeon was adhesions (in five patients), making the operation difficult. The other descriptions were inflammation (n 4), unclear plane between the gallbladder and liver bed (n 4), and bleeding (n 2). The anatomy was unclear in four cases, of which two were true anatomic variants with a separate right

3 1038 Nordin et al Table 2. Management in the Liver Unit: The Type of Bile Duct Injury and its Classification, Treatment, and Follow-up Subgroup Patient Type of Injury Class Treatment Follow-Up 1 1 Stricture in CHD/CBD E1 ERC, sphincterotomy, dilatations ( 3) 6yr5mo 2 Stricture in CHD E1 ERC sphincterotomy dilatations 5 6yr6mo 3 Stricture in CBD E2 ERC sphincterotomy dilatations and 12 mo stenting for 7 mo 2 4 Excision of CHD E2 Re-HJS into CHD 1 yr 2 mo 5 Excision of CHD, obstr. RHA E2 HJS into CHD 1 yr 10 mo 6 Excision of CHD/CBD E2 Re-HJS into CHD 8 mo 7 Excision of CHD E3 HJS into bifurcation 1 yr 8 mo 8 Stricture RHD, Stenosis CHD E4 HJS into two separate intrahepatic ducts 8 mo 3 9 Excision of CHD E2 Canalization, HJS into 2 separate ducts 3 mo 9mo later 10 Excision of CHD E3 HJS into bifurcation 2 yr 2 mo 11 Excision of CHD E3 Relaparotomy, recanalisation, waiting for 4 mo/dead definitive therapy 12 Excision of CHD/CBD E3 HJS into three separate intrahepatic ducts, 1yr11mo closure of duod. fistula 13 Excision of CHD E4 HJS into three separate intrahepatic ducts 2 yr 4 mo 14 Excision of CHD/CBD E4 HJS into bifurcation, re-hjs into two separate 6mo intrahepatic ducts 4 15 Stricture in CHD mx in left E1 PTC drainage and then liver transplantation 7 mo 16 Excision of CHD E2 Liver transplantation 7 mo/dead 17 Excision of CHD E3 Liver transplantation 2 yr 18 Excision of CHD E4 Liver transplantation 3 yr 10 mo NOTE. The patients are divided into subgroups according to the type of therapy: (1) endoscopic management, (2) HJS without need for prior external drainage, (3) HJS with need for preoperative external drainage period, (4) liver transplantation. Abbreviations: CHD, common hepatic duct; CBD, common bile duct; RHD, right hepatic duct; RHA, Right hepatic artery; ERC, endoscopic retrograde cholangiography; mx, multiple. hepatic segmental or bisegmental duct. In one patient, the operation was described as uneventful despite the existence of true right hepatic posterior duct variant, which might have contributed to the development of an E type injury (patient 9, Fig. 1). Intraoperative cholangiography was performed on four patients. In two of them, the injury was noted at the primary operation. In nine of the 11 patients without intraoperative cholangiography, the diagnosis of injury was delayed. The laparoscopy was converted to an open procedure in eight patients: five (28%) attributable to the immediate recognition of the bile duct injury, one caused by unclear anatomy during which the bile duct lesion was recognized, and two caused by bleeding during which the lesion remained unnoticed (patients 7 and 15). In eleven patients (61%), the diagnosis was delayed for a median of 6 days (range, 2 to 25). The clinical presentation of the injury included jaundice in three patients and abdominal pain with (n 7) or without (n 2) peritonitis. Three patients had no treatment before the referral. One patient was managed by percutaneous transhepatic cholangiography drainage. Fourteen patients had undergone 21 surgical operations altogether, followed by four endoscopic or radiologic interventions before referral (Table 1). Indications of referral. The median time period between diagnosis of the injury and referral was 79 (range, 0 to 2270) days. Only two patients were referred to our unit immediately after the recognition of the injury (9 and 14). Patients who developed cholangitis and end-stage liver disease (n 4) had the longest median time interval between injury recognition and referral, namely 1,747 days (range, 1196 to 2270). In the remaining 12 patients, a separate count gives a time interval of median 32 days (range, 1 to 72). The indication for referral was stricture (n 5), end-stage liver disease (n 4), bile duct lesion (n 3), definitive reconstruction (n 2), sepsis (n 1), peritonitis (n 1), bile leak (n 1), and suspicion of a retained stone in common bile duct (n 1).

4 Management of Major Iatrogenic Bile Duct Injuries 1039 Figure 1. Cholangiogram of a patient (9) with the common hepatic duct cut totally. There is a variant right duct (segments 6 and 7). Catheters are placed into the variant duct and common hepatic duct. Two metallic clips are placed into the cystic artery at the primary operation. The cystic duct was situated slightly below. The dissection of common hepatic duct and right hepatic duct junction, obviously with electrocoagulation, occurred after dividing the cystic duct and cystic artery. The Final Management The type of injury and its classification, the management after referral, and the duration of follow up period are listed in Table 2. The patients are divided into subgroups according to the final management. The location of the injury was below the hepatic bifurcation (type E1-E2) in half of the patients and at or above the bifurcation (type E3-E4) in the other half. Therapeutic endoscopic procedures were successful in three patients (Table 2, subgroup 1; patients 1 through 3) with distal injuries (E1-E2). Ten patients were managed by HJS. Five of them (Table 2, subgroup 2; patients 4 through 8) were operated shortly after referral because there was no evidence of bile leak or infection. The rest (Table 2, subgroup 3; patients 9 through 14) had biliary peritonitis and could not undergo surgery until the bile leak and biliary tree had been properly canalized and the inflammation subsided. One patient (11) succumbed before the definitive therapy because of sepsis and multiple organ failure. Four patients (Table 2, subgroup 4; patients 15 through 18) underwent liver transplantation (see later). The median hospital stay in our unit was 33 days (range, 10 to 164). There was no operative mortality, and only one reoperation was needed. Patient 14 developed biliary leak and sepsis after HJS, and successful re-hjs was performed 3 months later. At present, all patients of subgroups 1 through 3 who underwent treatment are alive with a median follow-up period of 20 (6 to 78) months from the last intervention. In one patient (9), few episodes of fever occurred during the early follow-up, and two other patients (4 and 6) had temporarily elevated transaminase values during the initial postoperative period. Liver transplantation. Patient 15 underwent elective LC complicated with severe, postoperative bleeding. During a laparotomy at the primary hospital the bleeding was controlled with a number of sutures placed at the hepatoduodenal ligament. During the following months, his state deteriorated slowly, and it was thought to be caused by a pre-existing liver disease because a suspicion of early primary biliary cirrhosis had been made already before the LC by liver biopsy. He was referred to our unit approximately 3.5 years after the LC. The patient had esophageal varices, and the liver biopsy showed stage 2-3 primary biliary cirrhosis and features of sclerosing cholangitis. PTC and computed tomography scan showed a stricture at the common hepatic duct and multiple strictures in the intralobar bile ducts and parenchymal atrophy of segments II-IV. The development of end-stage liver disease was obviously accelerated by the injury induced at LC. The bile duct stricture could not be dilated nor stented and the patient remained with PTC-drainage, which together with the significant portal hypertension and partial portal vein thrombosis were the indications for liver transplantation six months after referral. The postoperative course was free of rejections and infections. Subsequently, he developed a vasculitis-type disease affecting the most distal parts of his lower extremities. Vascular reconstructions were not necessary, and only necrotic skin lesions were debrided. He is alive with normal liver function tests 7 months after the transplantation. Patient 16 had her entire common hepatic duct excised during LC, and the lesion was immediately covered with HJS. The first episode of cholangitis occurred during the early postoperative days, and subsequently she underwent several attempts of PTC guided dilata-

5 1040 Nordin et al tions. Thereafter, surgery was never indicated because she became asymptomatic with conservative therapy. She was referred to the liver unit 6 years after the primary operation because of secondary biliary cirrhosis and recurrent variceal bleedings. She had undergone several variceal ligations without achieving a more permanent control of bleeding episodes, and at the final stage her condition deteriorated even further after a septic infection. The indications for liver transplantation were fulfilled, and she underwent the operation 3 months after referral. The patient had one cytomegalovirus (CMV) infection 2 months postoperatively and no rejection episodes. Initial recovery was followed by the development of Kaposi s sarcoma and she died 7 months after the transplantation. Patient 17 underwent elective LC in which her extrahepatic bile duct was partially excised. An HJS was performed immediately, but because of repeated stricture formation at the anastomosis, the bilioenteric bypass was repeated three times. She had numerous episodes of cholangitis and finally developed cirrhosis. She was referred to our unit 6.2 years after the LC. The indications for liver transplantation were secondary biliary cirrhosis, jaundice, and repeated episodes of cholangitis. She underwent the operation 2.5 months after referral. The postoperative course was devoid of any rejections or infections. She is doing well with normal liver function tests after 2 years of follow up. Patient 18 had his common hepatic duct excised during LC for acute cholecystitis. The lesion was noted 3 days later, and a heavily inflamed hepatic hilar area including three orifices of intrahepatic ducts was covered with a mucosal graft HJS (i.e., a pad of jejunal wall was sewn over the area without mucosa-to-mucosa anastomosis between the intestine and bile ducts). He had numerous episodes of cholangitis during the following months. Attempts to dilate the strictures by PTC failed and the Roux-en-Y limb was converted to include an enterocutaneous stoma for endoscopic access. The three intrahepatic ducts were dilated endoscopically several times but cholangitis did not subside and the stoma was kept open for future interventions. The infections and cholangitis episodes became even more serious, including colonization with skin bacteria. At referral, 3 years after the LC, he developed an abscess in the right liver lobe and microabscesses in the liver parenchyma. The indications for liver transplantation were rapidly progressing secondary biliary cirrhosis and jaundice. He underwent transplantation 2 months thereafter. He had no rejections and only a single episode of CMV pneumonia 3 months after the operation. This patient is in good health with normal liver function after 4 years of follow-up. The surgery, postoperative course and the length of intensive care unit (ICU) stay of these patients did not differ from other liver transplantation patients in the liver unit. The median time in hospital for transplanted patients was 89 days (range, 45 to 96) including the preoperative period. The cholangitis or septicemia associated with bile duct infection was controlled before the transplantation with wide range antibiotics if necessary. The immunosuppression of these patients consisted of triple therapy with cyclosporine or tacrolimus, azathioprine, and cortisone during the initial period. Thereafter, the drug regimen was tailored according to effectivity and side effects. At present, the immunosuppression of the remaining patients is based on cyclosporine or tacrolimus. Small doses of azathioprine are given if tolerated, and the cortisone is slowly withdrawn during the first 2 years unless liver function tests are elevated significantly. Discussion We present 18 patients referred to our unit with a major biliary complication from LC. The characteristics of injury recognition, number of attempts at repair, and referral pattern were comparable to earlier studies, in which the injury was diagnosed during the index operation in 15% to 33% of patients, 7,10,15-17 and the median delay for diagnosis was between 3 to 16 days in the rest of the patients. 10,15,18-21 Similarly, the time interval from diagnosis to referral varied from 3 to 32 days, 9,16,20 whereas in the present study it was 32 days if the patients with end-stage liver disease are excluded. The number of patients who underwent surgical attempts at repair in the primary hospital was slightly higher in the present study, namely 78% as compared with a range between 33% and 63% reported in earlier studies. 7,9,16-18,20 This reflects the selection bias of the injury types in the present study. There was a tendency for earlier detection of injury if intraoperative cholangiography had been performed at the primary operation. Although the value of peroperative imaging cannot be established from the results of the present study, it has to be emphasized that recent reports support the use of either intraoperative cholangiography or laparoscopic ultrasound to prevent or at least facilitate early detection of a bile duct injury. 3,22,23 The success rate of therapeutic endoscopy was 16% in patients with a single stricture from either failed suture repair or clip-induced necrosis and stenosis of

6 Management of Major Iatrogenic Bile Duct Injuries 1041 the duct wall in the present study. Other studies report nonsurgical management of major bile duct injuries to be successful in 19% to 22% of the cases referred. 17,20 The outcome of therapeutic endoscopy depends on the type of injury. In selected patients, the overall success may reach 93%. 13 The endoscopic or radiologically guided intervention may not be successful as a primary treatment in the more complex injuries 12 but it is certainly advantageous in recurrent anastomotic strictures or in patients not suitable for surgery. 12,17,24,25 The main option for correction of a bile duct injury is a Roux-en-Y HJS with tension-free mucosa-to-mucosa anastomosis. 24,26 This is a demanding operation, especially because the bile ducts are usually of normal diameter, and proper, viable anastomosis necessitates dissection high up in the hepatic hilum. The correct preoperative diagnosis, the choice and method of surgical repair, and the experience of surgeon determine the success of HJS. 7,8,12,24 In the present study, the surgeon entered the abdomen immediately when the injury was evident without preoperative attempts to secure the diagnosis in 67% of patients. Stewart and Way 12 reported only a 4% success rate for HJSs performed without prior evaluation of the entire hepatobiliary tree. The early repair of complex injuries is desirable, but if the detection of an injury is delayed, the chance for immediate cure is usually lost. 7,8,15 The inflammation, scar formation, and development of fibrosis takes several weeks to subside, during which the biliary flow should be controlled by other means. 7,8,12,15 Attempts at repair during this phase have a high rate of failure with poor outcome especially if repeated several times. 27 Injuries associated with laparoscopic approach are more likely to include bile leak with concomitant inflammation when compared with open cholecystectomy. 7 That seemed to be true in the present study as well. The initial sign of biliary injury was peritonitis in seven (38%) patients. Another aspect of surgical decision is the level of the biliary enteric anastomosis. Too distal anastomosis probably did contribute to the failure of the initial treatment of those patients who ended in the subgroup of acute infection and need for drainage at referral. These patients were more likely to require anastomosis involving the intrahepatic ducts than patients from the subgroup of stable situation at referral. In a retrospective review of 84 patients who underwent biliary enteric anastomosis for benign bile duct strictures the best results correlated with high level of anastomosis and with the degree of common bile duct dilatation independently of stricture location. 25 The high anastomosis is preferable because of the critical blood supply to the supraduodenal portion of biliary tree. 28 Eighty-two percent of patients operated before referral underwent a reoperation in our unit. This is consistent with an earlier study in which two thirds of patients with bile duct injuries, primarily those reconstructed in a local hospital later required repeat surgery in a referral center. 20 The difference in experience seems evident as shown in reports comparing success rate of HJS in tertiary centers vs. primary hospitals with results of 79% to 94% and 17% to 29%, respectively. 10,12,16,21 In recent reports the long-term success rate of HJS for bile duct injury was 94% to 100%. 7,13,17 A similar level of success was achieved in the present study as well, although the follow-up was shorter. The adoption of the principles of performing the HJS without tension, with mucosal adaptation into a vital bile duct with coring the base of segment 5, if necessary, seem to be associated with optimal results. 17,18,24,26 A failed bilioenteric reconstruction may lead to persistent cholangitis and end-stage liver disease within few years after the insult. 20,29 Johnson et al 17 found that the development of biopsy-proven hepatic fibrosis and early cirrhosis was associated with a significant delay in referral. The longer delay in the referral of transplanted patients was strikingly evident in the present study with a median interval of 4.8 years. At present only few studies report liver transplantation as the ultimate treatment of iatrogenic biliary tract lesions. In a study of 15 patients with complex bile duct injuries, one patient also had a vascular lesion resulting in hepatic failure, but the patient died before the planned transplantation. 30 One case has been published in which isolated right hepatic artery lesion at LC resulted in liver transplantation. 31 In a case report by Robertson et al, 32 a combined bile duct and vascular injury proceeded to biliary peritonitis and ischemic liver necrosis, which eventually necessitated transplantation. A combined vascular lesion may have influenced the outcome of primary attempts at repair in the present study and contributed to the development of end-stage liver disease in transplanted patients. 33,34 The four transplanted patients in the present study fulfilled the indications for liver transplantation as having an advanced chronic liver disease without alternative form of therapy nor absolute contraindication. 35 In addition, their United Network for Organ Sharing status was already 2B, and all of them had a Child-Pugh score of at least 10 (Child B) together with variceal bleeding or jaundice, indicating a need for imminent

7 1042 Nordin et al liver replacement. Liver transplantation did definitively improve their survival and quality of life. The rate of postoperative complications did not differ from other patient groups with cirrhosis in our unit. According to the European Liver Transplantation Registry 36 primary indications for liver transplantation include secondary biliary cirrhosis in 1% of all cases, a figure comparable to the patients in the present study. The survival of patients with secondary biliary cirrhosis following liver transplantation is 73% at 1 year and 69% at 5 years. In conclusion, major bile duct injury after LC is a potentially life-threatening condition resulting in a significant long-term morbidity. The main findings in this study were the association between the delay in referral and the development of end-stage liver disease necessitating liver replacement and the failure of primary attempt at repair obviously caused by the associated biliary peritonitis or sepsis and because of the choice of the method and technique in performing biliary enteric anastomosis. The early referral cannot be overemphasized because the primary surgeon, despite possessing a similar amount of technical ability, may not have the procedural knowledge of a surgeon who performs hepatobiliary operations frequently. Besides, the management of biliary injuries necessitates a multidisciplinary team, which is able to perform diagnostic and interventional radiological and endoscopic procedures as well as the necessary surgical operations including liver transplantation. References 1. Cuschieri A, Dubois F, Mouiel J, Houset P, Becker H, Buess G, et al. The European experience with laparoscopic cholecystectomy. Am J Surg 1991;161: The Southern Surgeons Club. A prospective analysis of 1518 laparoscopic cholecystectomies. N Engl J Med 1991;324: Fletcher DR, Hobbs MST, Tan P, Valinsky LJ, Hockey RL, Pikora TJ, et al. Complications of cholecystectomy: Risks of the laparoscopic approach and protective effects of operative cholangiography. Ann Surg 1999;229: MacFadyen BV, Vecchio R, Ricardo AE, Mathis CR. Bile duct injury after laparoscopic cholecystectomy. The United States experience. Surg Endosc 1998;12: Wherry DC, Marohn MR, Malanoski MP, Hetz SP, Rich NM. An external audit of laparoscopic cholecystectomy in the steady state performed in medical treatment facilities of the department of defense. Ann Surg 1996;224: Z graggen K, Wehrli H, Metzger A, Buehler M, Frei E, Klaiber C. Complications of laparoscopic cholecystectomy in Switzerland. A prospective 3-year study of 10,174 patients. Surg Endosc 1998;12: Lillemoe KD, Melton GB, Cameron JL, Pitt HA, Campbell KA, Talamini MA, et al. Postoperative bile duct strictures: Management and outcome in the 1990s. Ann Surg 2000;232: Strasberg SM, Hertl M, Soper NJ. An analysis of the problem of biliary injury during laparoscopic cholecystectomy. J Am Coll Surg 1995;180: Shah SR, Mirza DF, Afonso R, Mayer AD, McMaster P, Buckels JAC. Changing referral pattern of biliary injuries sustained during laparoscopic cholecystectomy. Br J Surg 2000;87: Carroll BJ, Birth M, Phillips EH. Common bile duct injuries during laparoscopic cholecystectomy that result in litigation. Surg Endosc 1998;12: Savader SJ, Lillemoe KD, Prescott CA, Winick AB, Venbrux AC, Lund GB, et al. Laparoscopic cholecystectomy-related bile duct injuries. A health and financial disaster. Ann Surg 1997; 225: Stewart L, Way LW. Bile duct injuries during laparoscopic cholecystectomy; factors that influence the results of treatment. Arch Surg 1995;130: Boerma D, Rauws EAJ, Keulemans YCA, Bergman JJGHM, Obertop H, Huibregtse K, Gouma DJ. Impaired quality of life 5 years after bile duct injury during laparoscopic cholecystectomy. A prospective analysis. Ann Surg 2001;234: Bismuth H. Postoperative strictures of the bile duct. In: The biliary tract, V. Edited by L.H. Blumgart. Pp Edinburgh: Churchill Livingstone Inc; dewit LT, Rauws EAJ, Gouma DJ. Surgical management of iatrogenic bile duct injury. Scand J Gastroenterol 1999;34(suppl 230): Doctor N, Dooley JS, Dick R, Watkinson A, Rolles K, Davidson BR. Multidisciplinary approach to biliary complications of laparoscopic cholecystectomy. Br J Surg 1998;85: Johnson SR, Koehler A, Pennington LK, Hanto DW. Longterm results of surgical repair of bile duct injuries following laparoscopic cholecystectomy. Surgery 2000;128: Davidoff AM, Pappas TN, Murray EA, Hilleren DJ, Johnson RD, Baker ME, et al. Mechanism of major biliary injury during laparoscopic cholecystectomy. Ann Surg 1992;215: Keulemans YC, Bergman JJ, dewit LTh, Rauws EA, Huibregtse K, Tytgat GN, et al. Improvement in the management of bile duct injuries? J Am Coll Surg 1998;187: Mirza DF, Narsimhan KL, Ferraz Neto BH, Mayer AD, McMaster P, Buckels JAC. Bile duct injury following laparoscopic cholecystectomy: referral pattern and management. Br J Surg 1997;84: Topal B, Aerts R, Penninckx F. The outcome of major biliary tract injury with leakage in laparoscopic cholecystectomy. Surg Endosc 1999;13: Flum DR, Koepsell T, Heagerty P, Sinanan M, Dellinger EP. Common bile duct injury during laparoscopic cholecystectomy and the use of intraoperative cholangiography. Arch Surg 2001; 136: Biffl WL, Moore EE, Offner PJ, Franciose R, Burch JM. Routine intraoperative laparoscopic ultrasonography with selective cholangiography reduces bile duct complications during laparoscopic cholecystectomy. J Am Coll Surg 2001;193: Bismuth H, Franco D, Corlette MB, Hepp J. Long term results of roux-en-y hepaticojejunostomy. Surg Gynecol Obstet 1978; 146: Tocchi A, Costa G, Lepre L, Liotta G, Mazzoni G, Sita A. The

8 Management of Major Iatrogenic Bile Duct Injuries 1043 long-term outcome of hepaticojejunostomy in the treatment of benign bile duct strictures. Ann Surg 1996;224: Strasberg SM, Picus DD, Drebin JA. Results of a new strategy for reconstruction of biliary injuries having an isolated right-sided component. J Gastrointest Surg 2001;5: Röthlin MA, Löpfe M, Schulmpf R, Largiadér F. Long-term results of hepaticojejunostomy for benign lesions of the bile ducts. Am J Surg 1998;175: Northover JMA, Terblanche J. A new look at the arterial supply of the bile duct in man and its surgical implications. Br J Surg 1979;66: Kozicki I, Bielecki K. Hepaticojejunostomy in benign biliary stricture influence of careful postoperative observations on long-term results. Dig Surg 1997;14: Madariaga JR, Dodson SF, Selby R, Todo S, Iwatsuki S, Startzl TE. Corrective treatment and anatomic considerations for laparoscopic cholecystectomy injuries. J Am Coll Surg 1994;179: Bacha EA, Stieber AC, Galloway JR, Hunter JG. Non-biliary complication of laparoscopic cholecystectomy. Lancet 1994; 344: Robertson AJ, Rela M, Karani J, Steger AC, Benjamin IS, Heaton ND. Laparoscopic cholecystectomy injury: An unusual indication for liver transplantation. Transpl Int 1998;11: Gupta N, Solomon H, Fairchild R, Kaminski DL. Management and outcome of patients with combined bile duct and hepatic artery injuries. Arch Surg 1998;133: Koffron A, Ferrario M, Parsons W, Nemcek A, Saker M, Abecassis M. Failed primary management of iatrogenic biliary injury: Incidence and significance of concomitant hepatic arterial disruption. Surgery 2001;130: Keeffe EB. Selection of patients for liver transplantation. In: Maddrey WC, Schiff ER, Sorrell MF. Eds. Transplantation of The Liver. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2001, pp The European Liver Transplantation Registry. Available at: Accessed May 15, 2002.

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