Liver Transplantation for Biliary Atresia: 19-Year, Single-Center Experience
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1 Liver Transplantation for Biliary Atresia: 19-Year, Single-Center Experience L Thomas Chin 1, Anthony M D Alessandro 1, Stuart J Knechtle 1, Luis A Fernandez 1, Glen Leverson 1, Robert H Judd 2, Elizabeth Spaith 1, Aydin Dalgic 3, Hans W Sollinger 1, Munci Kalayoglu 1 Objectives: In this study, we describe our 19-year experience with liver transplantation as the definitive treatment for congenital biliary atresia. Materials and Methods: We performed a retrospective study of 115 liver transplants from 1984 to 2003 in 85 patients with congenital biliary atresia. We determined the impact of era of transplantation ( and ), recipient age (< 1 and > 1), prior portoenterostomy, and type of surgery (whole-, reduced-, and split-liver transplant) on the outcome of the transplant. Results: Overall long-term survival is 83%. Survival is greater in the more-recent era. No impact of age or prior portoenterostomy on survival was seen. Split- liver grafts showed superior graft survival, whereas reduced-liver transplants had the worst overall graft survival. Conclusions: Our results confirm that long-term patient survival after liver transplantation for congenital biliary atresia is excellent. When required, partial liver grafts provide excellent longterm outcome. Keywords: Liver transplantation, Pediatric recipients, Biliary atresia Biliary atresia is a congenital disorder that causes obliteration or discontinuity of the extrahepatic biliary system in infants, resulting in obstruction of bile flow. Biliary atresia is caused by a progressive 1 Division of Organ Transplantation, Department of Surgery 2 Department of Pediatrics, University of Wisconsin Medical School, Madison, Wisconsin USA 3 Baskent University, Ankara, Turkey Address reprint requests to: Munci Kalayoglu, MD, Department of Surgery, University of Wisconsin Medical School, 600 Highland Avenue, H4/780 CSC, Madison, WI , USA Phone: Fax: munci@surgery.wisc.edu Experimental and Clinical Transplantation (2004) 2: sclerosing fibrous obliteration of the extra- and intrahepatic ductal system, which leads to secondary biliary cirrhosis and occurs in 1 in 15, 000 live births. Untreated, biliary atresia is almost universally fatal within 2 years, with a median survival of 8 months [1]. The initial treatment of biliary atresia is the Kasai procedure [2]. Approximately one third of patients undergoing Kasai portoenterostomy survive over 10 years without liver transplantation. Another one third have adequate bile drainage, but still develop complications of cirrhosis or recurrent cholangitis and require liver transplantation before the age of 10. For the remaining one third of patients, bile flow is inadequate after portoenterostomy, and the children develop progressive fibrosis and cirrhosis. Liver transplantation remains the only option for longterm survival in these last two groups of patients [3,4]. Since the first liver transplant for biliary atresia in 1963, improvements in organ preservation, immunosuppressive agents, and the use of reduced [5], split [6], and living donor [7] liver transplants have improved the results of liver transplantation and led to a marked improvement of the death rate among children waiting for liver transplantation. In this study, we reviewed our 19-year experience with orthotopic liver transplantation as the definitive treatment of congenital biliary atresia and investigated the impact of era of transplantation ( and ), recipient age (< 1 year old and > 1 year old), prior portoenterostomy, and type of surgery (whole-, reduced-, and split-liver transplant) on the outcome of the transplant. Materials and Methods We performed a retrospective review of our liver transplant database for patients who underwent transplantation for biliary atresia. This retrospective Copyright Başkent University 2004 Printed in Turkey. All Rights Reserved
2 L Thomas Chin et al. / Experimental and Clinical Transplantation (2004) 2: review was approved by the University of Wisconsin Institutional Review Board and a waiver of consent was granted. Surgical technique Recipients received a whole-, reduced-, or split-liver allograft as previously described [5,6,8]. No living donor liver transplants were performed. Reducedliver grafts were used beginning in In reduced- liver transplants, the left lateral segment (segments 2,3), the left lobe (segments 2,3,4) or the right lobe (segments 4-8) were transplanted. To maximize use of donor livers, a split-liver program was initiated in The ex vivo technique was used for all liver splitting procedures. The left lateral segment was used for the pediatric recipient and the trisegmental graft was placed in an adult. In general, our preference was to use whole-organ allografts for our pediatric patients. However, as patients deteriorated clinically, they were considered to be candidates for reduced- or split-liver transplantation. Liver preservation solutions included Ringer s lactate in 1 patient, Eurocollin s solution in 8 patients, and UW solution in the remainder. Immunosuppression Initially, immunosuppression consisted of a quadruple protocol in 21 patients and included induction therapy with antilymphocyte globulin mg/kg/day for 10 days and maintenance immunosuppression consisting of cyclosporine, azathioprine, and prednisone. Eventually, azathioprine maintenance was not used in an additional 21 patients. When tacrolimus became available, this was substituted for cyclosporine. OKT3 induction with tacrolimus maintenance was used in 4 patients. However, 3 patients rapidly developed posttransplant lymphoproliferative disorder, and this immunosuppressive protocol was discontinued. Our current immunosuppressive regimen consists of tacrolimus with a steroid taper to off over 3 to 6 months. The cohort of 85 patients was divided into two eras and The era included 49 patients. The era included 36 patients. During the first era, there were few centers with expertise in pediatric liver transplantation, and the patients transplanted reflected a significant number of out-of-state referrals as well as a number of donor organs shipped in from other regions of the country. This is reflected by the fact that in the first era, only 33% of the donor organs were procured in the state of Wisconsin, while in era two, 77% of the donor organs were procured in Wisconsin. Also during this time, with the growing number of programs performing pediatric liver transplantation, we saw a 3-fold increase in the average waiting time for transplantation, from 32 days in era 1 to 101 days in era 2. Otherwise, the recipient characteristics of age, pretransplant weight, sex, prior portoenterostomy, or prior abdominal surgery were not significantly different between the two eras. In addition, the second era reflects a change in the immunosuppressive regimen from quadruple immunosuppression to tacrolimus and prednisone maintenance therapy. Statistics Patient and graft survival rates were compared using the Kaplan-Meier statistics. Differences were detected using the log-rank test. The time of liver graft loss was determined as the time of retransplantation for graft failure or patient death. A P value of < 0.05 was considered significant. All analyses were performed using SAS statistical software. Results All patients referred for biliary atresia eventually underwent liver transplantation. Indications for transplantation included refractory ascites, coagulopathy, variceal bleeding, encephalopathy, failure to thrive, and recurrent cholangitis. One hundred fifteen liver transplants were performed in 85 patients with congenital biliary atresia at University of Wisconsin Children s Hospital from December 16, 1984 to March 27, Of the 85 recipients, 48 (56%) were less than one year of age at the time of transplant. Thirty-seven (44%) were greater than one year of age at the time of initial transplant. Fifty-nine recipients (69%) had previously undergone portoenterostomy, whereas 26 (31%) had no prior portoenterostomy. Seventy-nine recipients (93%) had undergone previous surgery. Six recipients (7%) had no prior abdominal surgery. Of the 81 patients transplanted, 83% are alive. Overall 1-, 2-, and 5-year actuarial survival rates were 90%, 88%, and 86%, respectively. The 1-, 2-, and 5-year graft survival rates were 73%, 72%, and 68%, respectively. The primary type of liver graft included 54 (64%)
3 180 L Thomas Chin et al. / Experimental and Clinical Transplantation (2004) 2: whole-liver transplants, 20 (24%) reduced-liver transplants, 10 (11%) split-liver transplants, and one (1%) cluster transplant. Of these transplants, 62 (76.5%) received a single graft, 12 patients required retransplantation once, 5 (6.2%) required retransplantation twice, and 2 (2.5%) required retransplantation 3 times. Indications for retransplantation were hepatic artery thrombosis, primary nonfunction, biliary tract complications, portal vein thrombosis, and vanishing bile duct syndrome. The mean waiting time was 56 days (range days). There were no deaths on the waiting list. The incidence of rejection was not significantly different between the two eras (P = 0.3, not shown). Comparing the two eras, liver graft survival remains significantly better in the more-recent era (Figure 1). There was no significant difference in liver graft survival between those with prior portoenterostomy and those without (Figure 2). When subanalyzed by type of transplant, split-liver grafts had significantly better survival than whole or reduced grafts (Figure 3). Reduced grafts had the worst overall survival. The 5-year graft survival was 92% for split-, 75% for whole-, and 45% for reduced-liver allografts. The causes of graft failure by graft type are shown in Table 1. Of note, primary nonfunction occurred in 5 reduced grafts. We feel this is reflective of our learning curve in reduced-liver grafts. Initially, we used the next available donor for liver reduction. A number of the graft failures occurred in steatotic livers or with extended preservation. Improvements in donor selection, including the routine use of donor liver biopsy, donor management, as well as surgical techniques for reduced-liver transplantation, led to the superior outcomes with split liver transplantation and zero percent primary nonfunction and hepatic artery thrombosis. Patient survival was significantly better in those receiving only one transplant. There was no signifi- P = Figure 1. Liver graft survival according to transplant era ( vs ) P = Figure 3. Liver graft survival according to type of transplant (whole vs reduced vs split) Table 1. Cause of graft loss by transplant type P = Figure 2. Liver graft survival with and without portoenterostomy Cause of Transplant Failure Whole Reduced Split Continued function 44 (67%) 12 (34%) 13 (93%) Chronic rejection 3 (4%) 4 (11%) 0 Primary nonfunction 0 5 (14%) 0 Biliary tract complications 1 (2%) 0 0 Hepatic artery thrombosis 11 (16%) 2 (6%) 0 Death with function 5 (7%) 6 (17%) 0 Other 1 (2%) 4 (11%) 0 Vanishing bile duct syndrome 1 (2%) 0 0 Portal vein thrombosis 0 2 (6%) 1 (7%)
4 L Thomas Chin et al. / Experimental and Clinical Transplantation (2004) 2: cant difference in patient survival by era, prior portoenterostomy, age (not shown), or type of liver graft (Figure 4) were not associated with a significant difference in survival. Early complications in our series of 85 patients included hepatic artery thrombosis requiring retransplant (17%), portal vein thrombosis (3%), bile leak or stricture (17%), reoperation (28%), bacterial infection (65%), viral infection (16%) and fungal infection (5%) within 6 months, and readmission in 60% of patients. Late complications included posttransplant lymphoproliferative disease in 9 patients (10%). As stated previously, however, a number of these cases, especially with early onset, were likely the result of the combined use of OKT3 and tacrolimus. Chronic rejection leading to graft loss occurred in 7 patients (8%). Renal failure remains a significant long-term problem, as 13 patients (15%) have developed renal insufficiency. Three of these patients have undergone successful kidney transplantation. Discussion P = Figure 4. Patient survival according to type of graft (whole vs reduced vs split) The two eras studied ( and ) are reflective of the evolution of our pediatric liver transplant program. One of the authors initial training as a pediatric surgeon led to his interest in liver transplantation as a therapy for congenital biliary atresia. At the inception of the University of Wisconsin liver transplant program in 1984, there were few centers with expertise in both portoenterostomy and liver transplantation. As a result, a number of centers outside the local area referred patients to the University of Wisconsin for liver transplantation. In addition, given the small number of pediatric liver transplant programs at that time, the majority of donor pediatric livers were imported from outside procurement organizations. As the number of pediatric liver transplant programs grew, we saw a smaller number of outside patient referrals as well as fewer outside donor referrals. This is reflected in the marked increase in waiting time in the era As a result, a program of partial liver grafts was initiated. Reduced-liver grafts were used successfully, although with a significant learning curve. The experiences gained with reduced grafts translated into improved outcomes with our split-liver transplant program and no waiting list mortality for biliary atresia patients awaiting liver transplantation. Given our success with split-liver transplantation, there has been no need to resort to living- donor liver transplantation as has been described in other programs [4,7,9]. The living-donor option may be necessary, however, depending upon the number of patients on the recipient list as well as the size and suitability of the donor pool for split-liver transplantation. Despite the long-term success of liver transplantation, Kasai portoenterostomy remains the preferred primary treatment for congenital biliary atresia. Ideally, portoenterostomy is performed within the first 10 weeks of life for optimal results. Liver transplantation as primary therapy would risk exposing the patient to additional potential early and late morbidity such as hepatic artery thrombosis, reoperation, infectious complications, effects of immunosuppression, chronic rejection, renal failure, and lymphoproliferative disease. The Western experience is that two thirds of patients will require liver transplantation within 10 years following portoenterostomy. Approximately one third of patients will have adequate biliary drainage after portoenterostomy and will have long-term survival without liver transplantation. Some series have reported over 60% 10-year survival after portoenterostomy [10]. The reported development of cirrhosis in long-term survivors after portoenterostomy has been reported to be from 10% to 40% [11,12]. Our series included 8 patients who required liver transplantation over 10 years after their portoenterostomy, including 1 patient who developed recurrent cholangitis and complications of portal hypertension almost 30 years later. Whether more of these long-term portoenterostomy successes
5 182 L Thomas Chin et al. / Experimental and Clinical Transplantation (2004) 2: will ultimately require liver transplantation remains to be seen. Conclusion In conclusion, excellent long-term survival can be achieved with orthotopic liver transplantation for congenital biliary atresia. Our algorithm for the management of biliary atresia is summarized in Figure 5. Kasai portoenterostomy remains the main treatment for biliary atresia. While two thirds are likely to fail, the Kasai often allows for a period of growth in these malnourished children that will facilitate finding appropriate-sized grafts. Those found to have cirrhosis or who develop complications such as recurrent cholangitis or portal hypertension should be referred for transplantation. The liberal use of partial grafts has virtually eliminated waiting list mortality. While our center has not employed living liver donation for pediatric patients, it may be a viable option for centers with less access to suitable cadaver donors. The combination of portoenterostomy and liver transplantation has improved the prognosis of biliary atresia from a uniformly fatal disease into a disease that can be successfully treated. References 1. Bates MD, Bucuvalas JC, Alonso MH, Ryckman FC. Biliary atresia: pathogenesis and treatment. Semin Liver Dis 1998; 3: Kasai, M, Suzuki S. A new operation for non-correctable biliary atresia, hepatic portoenterostomy. Shujutsu 1959; 13: Chardo C, Carton M, Spire-Bendelac N, Le Pmmelet C, Golmard JL, Aubert B. Prognosis of biliary atresia in the era of liver transplantation. Hepatology 1999; 25: Goss JA, Shackleton CR, Swenson K, Satou NL, Nuesse BJ, Imagawa DK, et al. Orthotopic liver transplantation for congenital biliary atresia: a 11 year, single center experience. Ann Surg 1996; 224: Figure 5. Algorithm for the management of biliary atresia Kalayoglu M, D'Alessandro AM, Sollinger HW, Hoffman RM, Pirsch JD, Belzer FO. Experience with reduced size liver transplantation. Surg Gynecol Obstet, 1990; 171: Kalayoglu M, D'Alessandro AM, Knechtle SJ, Hoffmann RM, Pirsch JD, Judd RH et al. Preliminary experience with split liver transplantation. J Am Coll Surg. 1996; 182: Broelsch CE, Whitington PF, Emond JC, Heffron TG, Thistlethwaite JR, Stevens L et al. Liver tranplantation in children from living related donors: surgical techniques and results. Ann Surg 1991; 214: Kalayoglu M, Stratta RJ, Sollinger HW, Hoffmann RM, D'Alessandro AM, Pirsch JD et al. Liver transplantation in infants and children. J Pediatr Surg 1989; 24: Fujita S, Tanaka K, Tokunaga Y, Uemoto S, Sano K, Manaka D et al. Living related liver transplantation for biliary atresia. Clin Transplantation 1993; 7: Nio M, Ohi R, Miyano T, Saeki M, Shiraki K, Tanaka K. Five and 10- year survival rates after surgery for biliary atresia: a report from the Japanese Biliary Atresia Registry. J Pediatr Surg 2003; 38: Hadzic N, Davenport M, Tizzard S, Singer J, Howard ER, Mieli- Vergani G. Long-term survival following Kasai portoenterostomy: is chronic liver disease inevitable? J Pediatr Gastroenterol Nutr. 2003; 37: Suruga K, Tsunoda S, Deguchi E, Kimura K, Miyano T. The future role of hepatic portoenterostomy as treatment of bliliary atresia. J Pediatr Surg 1992; 27:
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