Isolated Liver Transplantation in Infants with End-Stage Liver Disease Due to Short Bowel Syndrome

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1 LIVER TRANSPLANTATION 12: , 2006 ORIGINAL ARTICLE Isolated Liver Transplantation in Infants with End-Stage Liver Disease Due to Short Bowel Syndrome Jean F. Botha, Wendy J. Grant, Clarivet Torres, Angie K. Iverson, Debra L. Sudan, Byers W. Shaw Jr., and Alan N. Langnas Department of Surgery, Section of Organ Transplantation, University of Nebraska Medical Center, Omaha, NE Infants with short bowel syndrome (SBS) and associated liver failure are often referred for combined liver/intestinal transplantation. We speculated that in some young children, nutritional autonomy would be possible with restoration of normal liver function. Features we believed to predict nutritional autonomy include history of at least 50% enteral tolerance, age less than 2 yr, and no underlying intestinal disease. This report documents our experience with liver transplantation alone in children with liver failure associated with SBS. Twenty-three children with SBS and end-stage liver disease, considered to have good prognostic features for eventual full enteral adaptation, underwent isolated liver transplantation. Median age was 11 months (range, 6.5 to 48 months). Median pretransplant weight was 7.4 kg (range, 5.2 to 15 kg). All had growth retardation and advanced liver disease. Bowel length ranged from 25 to 100 cm. Twenty-three children underwent 28 isolated liver transplants. There were 14 whole livers and 14 partial grafts (five living donors). Seventeen patients are alive at a median follow-up of 57 months (range, 6 to 121 months). Actuarial patient and graft survival rates at 1 yr are 82% and 75% and at 5 yr are 72% and 60%, respectively. Four deaths resulted from sepsis, all within 4 months of transplantation, and 1 death resulted from progressive liver failure. Two allografts developed chronic rejection; both children were successfully retransplanted with isolated livers. Of 17 surviving patients, three require supplemental intravenous support; the remaining 14 have achieved enteral autonomy, at a median of 3 months (range, 1 to 72 months) after transplantation. Linear growth is maintained and, in many, catch-up growth is evident. Median change in z score for height is 0.57 (range, 4.47 to 2.68), and median change in z score for weight is 0.42 (range, 1.65 to 3.05). In conclusion, isolated liver transplantation in children with liver failure as a result of SBS, who have favorable prognostic features for full enteral adaptation, is feasible with satisfactory long-term survival. Liver Transpl 12: , AASLD. Received November 1, 2005; accepted December 22, See Editorial on Page 1040 Parenteral nutrition (PN) is the major supportive therapy for children with short bowel syndrome (SBS) until intestinal adaptation occurs and enteral autonomy is achieved. Children and infants with SBS are at risk of developing serious intestinal failure related complications before full intestinal adaptation has taken place. Catheter-related sepsis, loss of intravenous access, and intestinal failure (IF) associated liver disease may be life-threatening complications that result in treatment failure and the need for intestinal transplantation. Once liver disease develops, survival at 5 yr is 0% with most children dying within 2 yr of the onset of liver disease. When liver failure develops before weaning from PN has occurred, a vicious cycle of intolerance to feeding and progressive liver disease ensues. Ascites, bowel wall edema, and recurrent gastrointestinal bleeding as a result of impaired synthetic function of the liver and portal hypertension suppress bowel adaptation and intestinal function. Other factors, including bacterial overgrowth, bowel dysmotility, bile salt depletion, and Abbreviations: SBS, short bowel syndrome; PN, parenteral nutrition; IF, intestinal failure; ESLD, end-stage liver disease. Address reprint requests to Jean F. Botha, MD, University of Nebraska Medical Center, Omaha, NE Telephone: ; FAX: ; jbotha@unmc.edu. DOI /lt Published online in Wiley InterScience ( American Association for the Study of Liver Diseases.

2 LIVER TRANSPLANTATION FOR SHORT BOWEL SYNDROME 1063 recurrent central line infections, delay further weaning from PN. A small number of children referred for combined liver and intestinal transplant develop advanced PNassociated liver disease despite a seemingly adequate length of bowel; were it not for the presence of liver disease, these patients would in time possibly achieve enteral autonomy. We hypothesized that transplantation of the liver alone in these patients would remove the deleterious effects of liver failure, thus allowing time and optimal conditions for full intestinal adaptation to occur. We now report our experience with isolated liver transplantation in children with SBS- and IF-associated liver failure. PATIENTS AND METHODS Study Design This is a retrospective review of pediatric patients with SBS and end-stage liver disease (ESLD) who underwent isolated liver transplant at our institution. The goal of the study was to determine whether liver transplant alone is an appropriate treatment for selected patients with SBS- and IF-associated ESLD in terms of survival and nutritional outcome. Criteria that we believed would predict successful weaning from PN after liver transplant included a history of enteral tolerance of at least 50% of caloric requirements, age less than 2 yr (as most adaptation after neonatal resection has taken place by then), no less than 25 cm of small bowel, and no underlying intestinal disease. A secondary goal was to identify whether these criteria confirmed and what other factors might predict successful weaning from PN after isolated liver transplant. For this purpose, data collected included age at transplant, weight at transplant, and height and weight standard deviation scores (z scores) before transplant. Also examined were etiology of SBS, radiological small bowel length, presence of ileocecal valve, percentage of maximal enteral tolerance, prothrombin time, bilirubin, albumin, pediatric end-stage liver disease (PELD) score, type of transplant (whole vs. partial), and type of biliary anastomosis (Roux-en-Y choledochojejunostomy vs. duct-to-duct). Subjects The study population comprises 23 children who had been referred to our center for evaluation for combined liver and small bowel transplantation between 1995 and After thorough evaluation, it was determined that isolated liver transplant would be appropriate treatment for these patients, based on our criteria. All 23 children had SBS and ESLD. Median serum bilirubin was 19 mg/dl (range, 2.9 to 40 mg/dl), median prothrombin time was 17 seconds (range, 13.3 to 37 seconds), median serum albumin was 2.5 mg/dl (range, 2.1 to 3.0 mg/dl), and median PELD score was 30 (range, 18 to 44). The etiology of SBS represented the usual spectrum of diseases causing SBS in infants. All patients were severely growth-retarded as manifest by a median z score for height of 2.29 (range, 4.6 to 0.06) and a median z score for weight of 1.68 (range, 3.17 to 0.6). At the time of transplantation, the median age was 11 months (range, 6.5 to 48 months) and median weight of 7.5 kg (range, 5.2 to 15 kg). As part of the evaluation process, all patients underwent radiological assessment of residual small bowel length and transit time. Upper and lower endoscopies were also performed. The percentage of enteral tolerance was defined as the proportion of total caloric requirements that was tolerated by the enteral route, taking into account that caloric requirements for children with SBS are greater than those of healthy children. This included assessment of stool output and consistency as well as patient hydration and growth. As a group, the median enteral tolerance was 50% (range, 30 to 100%). The median small bowel length was 50 cm (range, 20 to 100 cm), and 13 patients had retained their ileocecal valves. After transplant, all patients were started on continuous tube feeding using an enteral formula of 15 to 20 calories per ounce. Tube feeds were advanced and PN weaned based on stool output, hydration, laboratory data, and growth. Immunosuppression consisted of tacrolimus and steroids for all patients except the first patient, who was treated with cyclosporine and continues to be on that drug. Typically, tacrolimus was administered on the first postoperative day, aiming for trough levels of ng/ml by the end of the first week. Statistical Analysis Patient and graft survival was calculated using the Kaplan-Meier method. Standard deviation scores were used to compare growth parameters before and at multiple time points after transplantation. Z scores were calculated using National Center for Health Statistics growth data. Z scores were compared using the Mann- Whitney U test, assuming non-gaussian distribution of the data. Data are expressed as median and range. Nominal data were compared using the Fisher exact test. RESULTS Twenty-three patients underwent 28 liver transplants of which 14 were whole organs and 14 partial livers (12 left lateral segments and two full left lobes). Five transplants were from living donors. The method of biliary reconstruction was by Roux-en-Y choledochojejunostomy in 12 cases and duct-to-duct anastomosis in 16. When a Roux-en-Y anastomosis was performed, the shortest possible Roux limb was used. This was usually cm long. T-tubes were not used for duct-to-duct anastomoses, but the anastomosis was usually constructed over a small stent that was either removed or advanced into the duodenum. Whenever possible, a duct-to-duct anastomosis was performed. Seventeen patients are alive at a median follow-up of 57 months (range, 6 months to 10 yr). Kaplan-Meier probability of patient survival at 1 and 5 yr is 82% and 72% respectively, whereas graft survival at 1 and 5 yr is

3 1064 BOTHA ET AL. Kaplan-Meier probability of patient and graft sur- Figure 1. vival. Figure 3. Standardized height z scores by time of follow-up. Data are expressed as median range. Figure 2. Outcome of 23 patients undergoing isolated liver transplant for short bowel syndrome and intestinal failure associated liver failure. Abbreviations: OLT, orthotopic liver transplant; PN, parenteral nutrition. 75% and 60%, respectively (Fig. 1). Six patients died after liver transplantation. Four of these patients died within 4 months of transplant from sepsis and multiorgan failure. One patient developed recurrent PN injury and was listed for combined liver and small bowel transplant but died while waiting. The last death was an unexpected event almost 2 yr after transplant in a patient who had recently been weaned from PN. Overall, five patients were retransplanted with a second isolated liver allograft, the indications for retransplant being hepatic artery thrombosis (1), massive hepatic necrosis (2), and chronic rejection (2) (Fig. 2). Postoperatively, bowel perforations occurred in three patients that required re-operation and repair with no long-term sequelae. One patient had portal vein thrombosis discovered by ultrasound on the first postoperative day; revision of the portal vein anastomosis was successful. There was one biliary stricture, which was managed successfully with percutaneous dilatation, and one child developed a perforated duodenal ulcer that required operation. Post-transplant lymphoproliferative disease occurred in two patients at 2 months and 7 yr after transplant. Both patients responded to low-dose cyclophosphamide therapy and temporary withdrawal of immunosuppression. Fourteen patients have been completely weaned from PN at a median of 3 months (range, 1 to 72 months) after transplant. Six of these patients meet all their nutritional requirements from oral intake; the remaining eight still require supplemental or full tube feeds. There were four children who have failed to be weaned from PN; three patients still require 20%, 25%, and 40% of their caloric intake in the form of PN, respectively, and the one child developed recurrent PN-associated liver failure and was listed for combined liver and intestinal transplantation. When differences between the successes and the failures were examined, there appeared to be no differences in median bowel length (56 vs. 45 cm, P 0.17) and percentage enteral tolerance (55% vs. 45%, P 0.06). A similar number of patients had retained ileocecal valve (P 1.0). Changes in the anthropometric parameters were assessed in the surviving children with at least 1 yr of follow-up. There were modest improvements in the individual height-forage and weight-for-age z scores over time. The median change in height-for-age z score was 0.57 (range, 4.47 to 2.68) over a 4-yr period. Similarly, the median change in weight-for-age z score was 0.42 (range, 1.65 to 3.05) over the same period, indicating maintenance of linear growth with some catch-up growth occurring in the first year after transplant (Figs. 3 and 4). In the patients who are alive, the current median albumin concentration is 3.9 mg/dl (range, 2.7 to 4.8 mg/dl), indicating adequate visceral protein stores. Four children have required autologous gut reconstruction. One child underwent a Bianchi procedure 2 yr after transplant followed by a serial transverse enteroplasty 3 yr later. He is currently off PN. The first patient in the series who is now more than 10 yr posttransplant underwent a Bianchi procedure 8 yr after transplant and is currently off PN. Gastric outlet obstruction occurred in a child who had previously had duodenal atresia repaired as a neonate and required reconstruction of his gastric outlet. A patient with necrotizing enterocolitis and a long transverse colon stricture underwent takedown of her end jejunostomy and resection of the colon stricture and jejunocolostomy 6 months after liver transplant was successfully weaned from PN.

4 LIVER TRANSPLANTATION FOR SHORT BOWEL SYNDROME 1065 Figure 4. Standardized weight z scores by time of follow-up. Data are expressed as median range. DISCUSSION Children with SBS are dependent on PN in order to survive while the remnant gut undergoes adaptation. Complications related to IF include loss of venous access, central line-related infections, and progressive liver failure that results in failure of PN. 1 Patients who have failed PN support due to the development of liver disease are considered for combined liver and intestinal transplantation. The youngest patients with ultra-short gut are the most susceptible to the development of PNassociated liver disease, which may develop in up to 50% of these patients. The etiology of liver disease in children on long-term PN is multifactorial; however, the role of intra-abdominal infections and sepsis is increasingly being recognized. Whatever the pathogenesis, once ESLD develops, the survival at 5 yr is 0%. 2 In some patients referred for liver and small bowel transplantation, ESLD has occurred despite a seemingly adequate small intestine. The presence of severe liver disease and portal hypertension has been shown to negatively impact the process of intestinal adaptation. 3 Portal hypertension results in malabsorption of sugar, fluid, and electrolytes. 4 Children with extrahepatic portal vein obstruction have shown improvement of nutrient absorption as well as improved growth after portal decompressive procedures. 5 Factors such as ascites, bowel wall edema, gastrointestinal bleeding, and luminal bile salt deficiency would be removed by an isolated liver transplant and allow time and improved conditions for complete enteral adaptation to occur. Small series and a few case reports have suggested that isolated liver transplantation for SBS- and IF-related liver failure is a feasible treatment option in selected patients with features suggestive of eventual enteral autonomy. Lawrence et al. 6 reported on five patients with SBS and ESLD who underwent six liver transplants. Of the four long-term survivors, two remain on PN. Case reports from Hassan et al. 7 and Gottrand et al. 8 confirm that long-term success can be achieved and that autologous gut reconstruction after isolated liver transplant is also feasible. Muiesan et al. 9 reported a series of five children with SBS and ESLD, three of whom underwent isolated liver transplant with the expectation of full enteral adaptation and eventual weaning from PN and two patients in whom combined liver and intestinal transplantation was indicated but, because of life-threatening liver failure, underwent liver transplantation with a sequential isolated intestinal transplant planned in the future. All three children transplanted with the expectation of eventual enteral adaptation were successfully weaned from PN. The two children who were bridged to intestinal transplant both died, one while waiting and the other after sequential isolated intestinal transplant. The criteria that we used to determine successful weaning of PN after liver transplant involve careful clinical assessment of bowel function, past and present. The key functional parameter that we use is maximum enteral tolerance, which is defined as that portion of total caloric requirement that has been tolerated by the enteral route at any time in the patient s history. This also takes into account the fact that caloric requirements in children with SBS are greater than those of healthy children. Enteral tolerance of 50% of required calories is the benchmark that we have used in considering children for isolated liver transplant. As can be seen from the children who have failed to be weaned from PN, they tended to have lower enteral tolerance than the group of patients who have successfully been weaned. Bowel length has always been a key predictor of weaning from PN in children with SBS. The lower limit of small bowel length (measured from the ligament of Treitz) which we considered likely to result in weaning from PN was 25 cm. Most children in this series had bowel lengths in the region of 50 cm. The patients who were unable to be weaned from PN have tended to have shorter bowel length than those who were successfully weaned. There are advantages to isolated liver transplant over combined liver and small bowel transplant. Lower immunosuppression is required, steroids can more easily be weaned, and organ availability is greater owing to standardized reduction techniques and the availability of living donor transplantation. A recent study by Fryer et al. 2 highlighted the disproportionately high waiting list mortality between liver transplant only candidates and liver-intestine candidates. Analysis of the Organ Procurement and Transplantation Network/Scientific Registry of Transplant Recipients database for 2003 revealed substantial waiting times for intestinal transplant candidates which translate into a waiting list death rate of 635 per 1,000 patient yr at risk. 10 In our experience, the waiting list mortality for combined liver and intestine candidates is 34% (unpublished data). We have previously reported our preliminary results of liver transplant alone in 11 children with SBS. 11 With 23 children, this report describes the largest experience of liver transplant alone in children with ESLD as a result of SBS- and IF-associated liver failure. Liver transplants were not performed with the intent of bridging patients to sequential small bowel transplantation, as proposed by Muiesan et al., 9 but rather with the expectation that these children could be weaned from

5 1066 BOTHA ET AL. PN in the presence of normal liver function and the absence of portal hypertension. Seventeen of 24 patients are alive after liver transplant; in most of the survivors, PN has been weaned, and this independence from PN is sustained over the long term with most patients meeting their caloric requirements via the enteral route. Of the patients who are still receiving PN, the first had only 30 cm of small bowel; the second was weaned from PN in hospital but has been placed back on PN after discharge due to the parents refusal of continuous tube feeds. The third patient was also successfully weaned from PN in hospital but experienced significant growth failure at home (possibly due to social circumstances at home) and was restarted on PN. Growth after transplant has been maintained, and when compared at different time points after transplant, there appears to be some catch-up growth in the first year after transplant; thereafter, it stabilizes and growth velocity seems to be maintained with little evidence of catch-up growth. This is difficult to explain but may be due in part to less frequent physician contact after the first year and therefore less intensive nutritional management. This series provides compelling evidence that in carefully selected patients with SBS and ESLD with favorable prognostic features for eventual enteral autonomy, liver transplant alone can provide the time and the optimal circumstances required for full intestinal adaptation to take place. Survival is acceptable, and independence from PN is durable. REFERENCES 1. Buchman AL, Scolapio J, Fryer J. AGA technical review on short bowel syndrome and intestinal transplantation. Gastroenterology 2003;124: Fryer J, Pellar S, Ormond D, Koffron A, Abecassis M. Mortality in candidates waiting for combined liver-intestine transplants exceeds that for other candidates waiting for liver transplants. Liver Transpl 2003;9: Weber TR, Keller MS. Adverse effects of liver dysfunction and portal hypertension on intestinal adaptation in short bowel syndrome in children. Am J Surg 2002;184: Jacobs DL, Lof J, Quigley EM, Spanta AD, Rikkers LF. The effect of mesenteric venous hypertension on gut motility and absorption. J Surg Res 1990;48: Kato T, Romero R, Koutouby R, Mittal NK, Thompson JF, Schleien CL, Tzakis AG. Portosystemic shunting in children during the era of endoscopic therapy: improved postoperative growth parameters. J Pediatr Gastroenterol Nutr 2000;30: Lawrence JP, Dunn SP, Billmire DF, Falkenstein K, Vinocur CD, Weintraub WH. Isolated liver transplantation for liver failure in patients with short bowel syndrome. J Ped Surg 1994;29: Hassan KO, Beath SV, McKiernan PJ, Kelly DA, Clarke SE, Pimpilwar A, Bianchi A, DeVille de Goyet J. Difficult management choices for infants with short bowel syndrome and liver failure. J Pediatr Gastroenterol Nutr 2002;35: Gottrand F, Michaud L, Bonnevalle M, Dubar G, Pruvot F, Turk D. Favorable nutritional outcome after isolated liver transplantation for liver failure in a child with short bowel syndrome. Transplantation 1999;67: Muiesan P, Dhawan A, Novelli M, Mieli-Vergani G, Rela M, Heaton N. Isolated liver transplant and sequential small bowel transplantation for intestinal failure and related liver disease in children. Transplantation 2000;69: Harmon WE, McDonald RA, Reyes JD, Bridges ND, Sweet SC, Sommers CM, Guidinger MK. Pediatric transplantation. Am J Transplant 2005;4(Pt. 2): Horslen, SP, Sudan DL, Iyer KR, Kaufman SS, Iverson AK, Fox IJ, Shaw BW, Langnas AN. Isolated liver transplantation in infants with end-stage liver disease associated with short bowel syndrome. Ann Surg 2002;235:

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