Living Related Liver Transplantation for Acute Liver Failure in Children
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1 ORIGINAL ARTICLES Living Related Liver Transplantation for Acute Liver Failure in Children Sukru Emre, Myron E. Schwartz, Benjamin Shneider, Joanne Hojsak, Leona Kim-Schluger, Thomas M. Fishbein, Stephen R. Guy, Patricia A. Sheiner, Neal S. LeLeiko, Audrey Birnbaum, Frederick J. Suchy, and Charles M. Miller The mortality rate among children with acute liver failure (ALF) on the waiting list for liver transplantation is high. We present our experience with living related donor liver transplantation (LRD-LT) in children who required urgent transplantation for ALF. Between December 1995 and July 1997, 6 children underwent LRD-LT for ALF. Cause of liver failure, recipient and donor demographics, clinical and laboratory data, surgical details, complications, and 6-month and 2-year graft and patient survival were recorded. Five boys and 1 girl received left lateral segment grafts from their parents. The mean age was years (range, 1 to 9 years). ALF was caused by Wilson s disease in 1 patient and sickle cell intrahepatic cholestasis syndrome in 1 patient; in 4 patients, the cause was unknown. All patients had mental status changes; 2 were on life support. Mean pretransplantation liver function test values were: alanine aminotransferase, U/L (normal, 1 to 53 U/L), total bilirubin, mg/dl (normal, 0.1 to 1.2 mg/dl), prothrombin time, seconds (normal, 10.8 to 13.3 seconds), international normalized ratio, (normal F 2), and fibrinogen, mg/dl (normal, 175 to 400 mg/dl). The donors were 5 mothers and 1 father. The mean donor age was years (range, 19 to 40 years). No donor required blood transfusion, and no donor had any early or late postoperative complications. The donors mean hospital length of stay was 5 days. In five cases, grafts were blood group compatible; 1 child received a blood group incompatible graft. All grafts functioned immediately. No patient had hepatic artery or portal vein thrombosis or biliary complications. The child who received a mismatched graft died of infection of the brain caused by Aspergillus spp at 22 days posttransplantation with a functioning graft. The child with ALF caused by sickle cell intrahepatic cholestasis syndrome developed outflow obstruction 3 months posttransplantation and required retransplantation; he eventually died of vascular complications related to his primary disease. Four children are alive at a mean follow-up of 27 months (range, 14 to 36 months). LRD-LT for children with ALF facilitates timely transplantation without drawing on cadaveric donor resources. The established safety record of LRD-LT made this option appealing to both physicians and parental donors. Copyright 1999 by the American Association for the Study of Liver Diseases Acute liver failure (ALF) is a life-threatening syndrome defined in the pediatric patient population as the acute onset of severe hepatic dysfunction, with or without encephalopathy, developing within 8 weeks from the first signs of illness in a patient without underlying chronic liver disease. 1 ALF has a high mortality without liver transplantation. 1-3 In children with ALF, the mortality rate on the transplant waiting list is 20%. 4 For all patients, the shortage of donor organs limits the timely availability of livers; for children in particular, the availability of cadaveric donors is unpredictable. In children with chronic liver disease, living related donors have proved to be a viable option for obtaining liver grafts in a timely fashion and improving the outcome of liver transplantation. In children with ALF, however, there is limited experience with living related donor liver transplantation (LRD-LT). Here we present our experience in children who underwent LRD-LT for ALF. Methods Between December 1995 and July 1997, 6 children underwent LRD-LT for ALF. ALF was defined as severe From the Recanati/Miller Transplantation Institute, Mount Sinai Medical Center, New York, NY. Presented in part before the annual meeting of the American Society of Transplant Surgeons, Chicago, IL, May 14, Address reprint requests to Sukru Emre, MD, Mount Sinai Hospital, Box 1104, One Gustave L. Levy Place, New York, NY Copyright 1999 by the American Association for the Study of Liver Diseases /99/ $3.00/0 Liver Transplantation and Surgery, Vol 5, No 3 (May), 1999: pp
2 162 Emre et al impairment of liver function, with or without encephalopathy, in association with hepatocellular necrosis, developing within 8 weeks of the first signs of illness in a patient without underlying chronic liver disease. 1 Children were put on the waiting list for cadaveric organs while their parents were evaluated for possible candidacy as donors. If any appropriate cadaveric liver became available during this process, cadaveric liver transplantation was performed. Cause of liver failure, recipient and donor demographics, pretransplantation clinical and laboratory data, surgical details of the donor and recipient procedures, complications, and 3-month and 1-year graft and patient survival were recorded. Long-term follow-up data on donors were obtained by telephone interview. Donors were selected based on blood type, liver function, negative serological test results (hepatitis B virus, hepatitis C virus, HIV), physical examination, psychosocial evaluation that included alcohol and substance abuse, and left lateral segment volume as assessed by computed tomography. All donors gave informed consent. Graft volume matching was calculated using graft volume to recipient body weight ratio (graft volume in cubic milliliters). A graft volume to recipient body weight ratio of 1 was considered the lower limit for safety; practically, at least 1 g of liver tissue for each 100 g of recipient body weight. Angiography to evaluate the hepatic artery anatomy was not performed for two reasons: first, to decrease donor morbidity, and, second, we believe that the anatomic variations of the left hepatic artery are limited and can be dealt with during the surgical procedure. Multiple arteries to the left lateral segment of the liver were not considered a contraindication for donation. Donor and recipient operations were started simultaneously and performed using techniques described previously. 5-7 We did not use intracranial pressure monitoring in recipients. In the donors, the Pringle maneuver was not used during the parenchymal transection. The donor s left lateral segment was removed when the recipient team was ready to remove the diseased liver to keep cold ischemia time to less than 1 hour. The recipient operation was performed using piggyback technique. None of the cases required extension grafts. The hepatic artery anastomosis was performed using 9/0 nylon under an operating microscope. In 5 patients, immunosuppression consisted of tacrolimus and steroids. In 1 patient who received a blood group incompatible graft, initial immunosuppression was OKT3, cyclosporine, cyclophosphamide, and steroids; this patient also received exchange transfusions to decrease anti-b titers pretransplantation. Statistical analysis was performed with the log-rank test. Results are expressed as mean standard deviation. Results Five boys and 1 girl received left lateral segment grafts from their parents. Their mean age was years (range, 1 to 9 years). Five patients received blood type matched grafts; in the sixth patient, the donor was blood type B and the recipient was type O. ALF was caused Wilson s disease in 1 patient and sickle cell intrahepatic cholestasis syndrome in 1 patient; in 4 patients, the cause was unknown. All patients were in the pediatric intensive care unit pretransplantation; 2 were on life support. All had mental status changes (coma stages 1 to 4). Mean pretransplantation liver function test values were: alanine aminotransferase, U/L (normal, 1 to 53 U/L); total bilirubin, mg/dl (normal, 0.1 to 1.2 mg/dl); prothromin time, seconds (normal, 10.8 to 13.3 seconds); international normalized ratio, (normal 2); and fibrinogen, mg/dl (normal, 175 to 400 mg/dl). The mean interval from the time patients were listed to the time they underwent liver transplantation was 3 days. The donors were 5 mothers and 1 father. Their mean age was years (range, 19 to 40 years). None of the donors required blood transfusion. Mean donor hospital stay was 5 days. Average follow-up time is months (range, 17 to 36 months). None of the donors has had any early or late postoperative complications. Recipient characteristics and surgical details are listed in Table 1. All grafts functioned immediately. There was no hepatic artery or portal vein thrombosis and no biliary complications. Within 10 days, all patients were extubated and showed neurological recovery. None of the children had neurological sequela after LRD-LT. One patient required reexploration 2 days after transplantation because of intra-abdominal bleeding. The child who received a mismatched graft from his father had a difficult postoperative course. He developed a severe rejection episode on postoperative day 7, which was treated with steroid recycle. His postoperative course was further complicated with pneumonia; he eventually died of infection of the brain caused by Aspergillus spp and subarachnoid hemorrhage at 22 days posttransplantation with a functioning graft. The child with ALF caused by sickle cell intrahepatic cholestasis syndrome developed outflow obstruction 3 months after LRD-LT. A venogram showed normal inferior vena cava and he-
3 LRD-LT for ALF in Children 163 Table 1. Recipient Characteristics and Surgical Details Age (yr) Sex Cause INR Coma Stage Donor Liver/ Recipient Body Weight Ratio Cold Ischemic Time (min) Warm Ischemic Time (min) 4 M Wilson s NA M Unknown M Sickle cell M Unknown M Unknown F Unknown Abbreviations: INR, international normalized ratio; PRBC, packed red blood cells; NA, not available. PRBC (units) patic veins without obstruction and no pressure gradient. Because there was no technical problem to explain outflow obstruction, this problem was attributed to his sickle cell disease. He required retransplantation and eventually died of vascular complications related to his primary disease 6.5 months after the first transplantation. Two patients had acute cellular rejections. One, the patient who received the mismatched graft, experienced rejection 8 days posttransplantation; another patient experienced rejection on postoperative day 40. The average hospital length of stay for recipients was days (median, 23.5 days). Four children are alive and well at a mean of 25 months (range, 17 to 36 months). Three-month actual graft and patient survival rates were both 83.3%. Oneyear actual graft and patient survival rates were both 66.7%. Discussion Although 8% to 33% of the patients with ALF recover with medical treatment, liver transplantation is the only treatment option for the majority of patients. 1-3,8 Once a decision is made to proceed with liver transplantation, patients with ALF usually have a limited time before they develop lifethreatening complications, such as brain swelling/ herniation or sepsis. Finding a donor liver in a timely fashion in this setting is of prime importance for a successful outcome. Moreover, it is well known that small-size grafts, especially for children aged younger than 5 years, are more limited in availability than adult grafts. 4 Although this problem has been somewhat alleviated by the use of reduced and split-liver grafts in small children, mortality among children with ALF on the waiting list is nevertheless increasing worldwide. 2,3,9 LRD-LT was originally developed as a technique for children with chronic end-stage liver disease. LRD-LT provides many advantages to the recipient, including high-quality grafts with very short ischemia time and timely availability. In our center, 29 children have undergone liver transplantation for ALF. In addition to the 6 patients described here, 14 patients received whole-liver grafts, 3 patients received split-liver grafts, and 6 patients received reduced-size liver grafts. Among the 23 patients who waited for cadaveric grafts, the average waiting time was 3.8 days, compared with 3 days of waiting time for children who ultimately underwent LRD-LT. For recipients of reduced or split grafts, 3-month and 1-year graft and patient survival rates were 66.6% each (3 of 9 patients died of sepsis within 3 months posttransplantation; 6 of 9 patients are alive and well). For recipients of whole-liver grafts, 3-month and 1-year graft survival rates were 64.2% each, and 3-month and 1-year patient survival rates were 71.4% each. With this review, we are not attempting to prove that LRD grafts are superior to cadaveric grafts. We do not argue that LRD-LT should be a routine alternative to cadaveric liver transplantation with either whole, reduced-size, or split grafts. We believe that LRD-LT is a good adjunct to our surgical repertoire that gives an opportunity to deal with this very difficult clinical problem to save patients lives. Since we began to use LRD-LT for ALF cases, the pediatric waiting list mortality rate for ALF in our center is 9%, less than half that nationwide. Except for reports from Japan, 10,11 there is limited information on use of LRD-LT for ALF. In
4 164 Emre et al countries such as Japan, where cadaveric donors have not been available, LRD-LT is more easily justified. In the United States, where cadaveric donors are available, ethical problems must be addressed to justify this procedure. In general, the most important ethical dilemma with LRD-LT is that the process subjects a healthy person to a major operation. Presently, more than 1500 living related donor resections have been performed worldwide, with two reported deaths; one death from pulmonary embolus, 12 and one death attributed to anesthesia. The patient with the pulmonary embolus was obese and a heavy smoker and was probably a poor surgical candidate. In neither case were there any technical complications related to the procedure (Xavier Rogiers, personal communication, September 1998). Both cases point out the importance of donor evaluation and selection in preventing living donor mortalities. Overall, at our center, we have performed 26 LRD-LT, including these 6 patients with ALF. In 24 cases, the left lateral segment was used. In 2 cases, left lobe grafts were used. There were no complications or deaths in the donors, and no requirement for transfusion during the donor operations. The mean hospital length of stay for all living related donors at our center, including those described here, was 5 days. Our average follow-up on these living related donors is nearly 2 years, with no long-term morbidity. All donors resumed their routine activities within 3 months after their surgery. These results, along with results from the International Living Related Liver Transplant Registry (Xavier Rogiers, personal communication, September 1998) and from other centers, 13,14 confirm the general safety of the donor operation. The other major ethical concern regards the potential for coercion. Parents who are considering donating a segment of liver to a child in ALF must make their decision quickly. The urgency increases the pressure on the donor and increases the risk that a decision will be coerced by other family members, or even by the medical team. Participation of social workers and psychiatrists in the donor s workup is critical to minimize this risk. Conversely, the benefits to the living donor should not be discounted. The welfare of parent and child are inextricably intertwined; the suffering of a child is borne by the parents as well. Furthermore, the opportunity to provide a lifesaving graft is viewed as highly desirable, and many families actively seek out centers that provide this option. Tanaka et al 15 reported 13 cases of LRD-LT across blood groups. With an immunosuppressive protocol that consisted of low-dose steroids, tacrolimus, and induction OKT3, along with plasma exchange, there was no increased incidence of rejection, and no patient developed lethal infectious complications. Our experience with LRD-LT across blood groups was different, unfortunately. The child who received a mismatched graft developed both severe rejection and lethal infection. Although we cannot rule out a role for high-dose immunosuppression in the development of lethal infection, this child s critical condition before transplantation also had a role in his dismal outcome. There have been two reports of liver transplantation in patients with sickle cell disease. 16,17 These reports highlight the need for preoperative precautions, such as prevention of hypothermia and acidosis and maintenance of a hemoglobin S level less than 25% to prevent sickle cell crisis on reperfusion and in the early postoperative period. In these reports, sickle cell disease was a comorbid condition, rather than the primary cause of liver failure. In our patient, sickle cell intrahepatic cholestasis syndrome was the indication for transplantation. Although every precaution to prevent sickling was taken, this patient developed outflow obstruction attributed to sickling and required retransplantation 3 months after the first transplant. This patient developed intrahepatic segmental hepatic artery thrombosis and liver necrosis and died of sepsis 6 months after the initial transplant. In summary, in our small series, 5 of 6 children (83.3%) who underwent LRD-LT for ALF survived 6 months, and 4 of 6 children (66.7%) are still alive at a mean follow-up of 27 months (range, 14 to 36 months). Donors did not experience any early or late complications and resumed their routine activities within 3 months. The established safety record of LRD-LT made this option appealing to both physicians and the parental donors. Based on these results, we conclude that LRD-LT for children with ALF facilitates timely transplantation without drawing on cadaveric donor resources. References 1. Bismuth H, Samuel D, Castaing D, Williams R, Pereira SP. Liver transplantation in Europe for patients with acute liver failure. Semin Liver Dis 1996;16:
5 LRD-LT for ALF in Children Bhaduri BR, Mieli-Vergani G. Fulminant hepatic failure: Pediatric aspects. Semin Liver Dis 1996;16: Rivera PT, Moreno J, Skaff C, McDiarmid S, Vargas J, Ament ME. Delayed encephalopathy in fulminant hepatic failure in the pediatric population and the role of liver transplantation. J Pediatr Gastroenterol Nutr 1997; 24: Annual Report of the US Scientific Registry for Transplant Recipients and the Organ Procurement and Transplantation Network Transplant Data: UNOS, Richmond, VA, and the Division of Transplantation, Office of Special Programs, Health Resources and Services Administration, US Department of Health and Human Services, Rockville, MD. 5. Tanaka K, Uemoto S, Tokunaga Y, Fujita S, Sano K, Nishizawa T, et al. Surgical techniques and innovations in living related liver transplantation. Ann Surg 1993; 217: Heffron TG, Emond JC. Living related liver transplantation. In: Busuttil RW, Klintmalm GB (eds). Transplantation of the liver. Philadelphia: Saunders, 1996: Morimoto T, Ichimiya M, Tanaka A, Ikai I, Yamamato Y, Nakamura Y, et al. Guidelines for donor selection and an overview of the donor operation in living related liver transplantation. Transplant Int 1996;9: McCashland TM, Shaw BW, Tape E. The American experience with transplantation for acute liver failure. Semin Liver Dis 1996;16: Tan KC, Mondragon RS, Vougas V, Mieli-Vergani G, Heaton ND, Mowat AP, et al. Liver transplantation for fulminant hepatic failure and late-onset hepatic failure in children. Br J Surg 1992;79: Fuchinoue W, Tanaka K, Takasaki K, Hashimoto E, Kawai T, Nakajma I, et al. Living related liver transplantation for fulminant hepatic failure. Transplant Proc 1997;29: Terajima H, Tanaka K, Okajima K, Inomata Y, Yamaoka Y. Timing of transplantation and donor selection in living related liver transplantation for fulminant Wilson s disease. Transplant Proc 1995;27: Sterneck MR, Fischer L, Nischwitz U, Burdelski M, Kjer S, Latta A, et al. Selection of the living liver donor. Transplantation 1995;60: Morimoto T, Tanaka A, Ikai I, Yamamoto Y, Nakamura Y, Takada Y, et al. Donor safety in living related liver transplantation. Transplant Proc 1995;27: Heffron TG, Langnas AN, Fox IJ, Antonsin DN, Mack DR, Zetterman R, et al. Preoperative evaluation of the living related donor in pediatric living related liver transplantation. Transplant Proc 1995;27: Tanaka A, Tanaka K, Kitai T, Yanabu N, Tokuka A, Sato B, et al. Living related liver transplantation across ABO blood groups. Transplantation 1994;58: Lang T, Berquist WE, So SK, Cox KL, Rich EJ, Vichinsky E, et al. Liver transplantation in a child with sickle cell anemia. Transplantation 1995;59: Kindscher JD, Laurin J, Delcore R, Forster J. Liver transplantation in a patient with sickle cell anemia. Transplantation 1995;60:
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