Archives ofDisease in Childhood 1995; 72: 447-451 447

CURRENT TOPIC Arch Dis Child: first published as 10.1136/adc.72.5.447 on 1 May 1995. Downloaded from The future of small bowel transplantation

Deirdre A Kelly, John A C Buckels

Although transplantation of solid organs such Indications for small bowel as kidney and have been established since transplantation the 1970s and 1980s, the future of small bowel Small bowel transplantation should be con- transplantation as treatment for intestinal fail- sidered for all children with irreversible ure is only just evolving. Early clinical experi- intestinal failure who are dependent on par- ence was almost universally unsuccessful but enteral nutrition for survival and in whom all recent developments in surgical technique, attempts to improve intestinal adaptation have immunosuppression, and postoperative man- been unsuccessful. Potential candidates may agement have improved outcome with a 50% require small bowel transplantation alone or survival in at least 100 operations.' combined with a liver transplant. Small intestinal transplantation was first The current indications for isolated small demonstrated to be technically feasible in bowel transplantation include: (1) loss of animals in 1902,24 and in humans in the vascular access with normal liver function and 1980s,5-7 but it was not until the Pittsburg histology and (2) intractable gastrointestinal group initiated a programme of small bowel fluid loss. The current indications for com- transplantation using the novel immuno- bined small bowel/ are: (1) suppressant agent FK5068-12 that significant irreversible liver disease secondary to TPN; (2) progress was made. loss of vascular access with evidence of signifi- cant liver disease; and (3) inborn errors of liver metabolism leading to small bowel failure (for Intestinal failure example, protein C, S deficiency).24 25 Intestinal failure is defined as the inability of At the moment it is hard to justify small the to absorb sufficient solute to bowel transplantation in those patients who are maintain nutrition and/or positive fluid and successfully managed on TPN, although it is electrolyte balance.'3 It is more common in possible that in the future social, psychological, http://adc.bmj.com/ children, and the main causes are congenital and cost pressures may increase the indications abnormalities of the intestine and the short gut for transplantation. The contraindications syndrome secondary to neonatal surgery for a include uncontrolled sepsis or malignancy else- number of conditions (table). where in the body, HIV infection and severe Current treatment for intestinal failure is cerebral, cardiac, or respiratory disease. total parenteral nutrition (TPN) and many Congenital immunodeficiency may be a par- patients may be successfully maintained in this ticular contraindication because of the devel- on October 4, 2021 by guest. Protected copyright. way by specialist units.l4-16 Although success- opment of severe graft versus host disease ful provision of TPN at home has greatly (GVHD) from donor lymphocytes contained improved the outcome and quality of life for within the intestinal graft.26 Currently there children with short bowel syndrome, morbidity are no age or size limitations, although in prac- remains significantl7-'9 and the financial cost tice donor availability may preclude intestinal high.20 There are many complications which transplantation in very small infants. include cholestasis, cholelithiasis, pulmonary embolism, loss of vascular access, and recur- rent catheter sepsis.21-23 Patient selection and preparation Death in childhood is related to the develop- TIMING ment of liver dysfunction, as more than As quality of life may be acceptable for many 40% ofpatients with complete intestinal failure children maintained on parenteral nutrition will develop severe liver disease within two the timing of this operation may be difficult. Liver Unit, Birmingham years.22 Furthermore, the difficulty in obtaining suit- Children's Hospital, able age and size matched donors for very Ladywood Middleway, small children means a lengthy wait for a suit- Birmingham B16 8ET Causes ofintestinalfailure in childhood able organ. In Pittsburg 37% of patients died D A Kelly while awaiting small bowel transplantation.9 Short gut syndrome secondary to neonatal surgery for: Department of Intestinal atresia We have recently evaluated 17 children Surgery, Queen Gastroschisis (aged 4 months to 13 years) for small bowel Elizabeth Hospital, Volvolus Birmingham Necrotising enterocolitis transplantation. Ten children were referred J A C Buckels Aganglionosis with liver disease and seven with loss ofvenous Microvillus inclusion disease access. of children 11 died Correspondence to: Autoimmune enteropathy In this group pre- Dr Kelly. operatively (seven were too ill to place on the 448 Kelly, Buckels

transplant list and four died waiting for a isolated small bowel transplantation or com- donor. The children with the highest plasma bined liver and small bowel transplantation. bilirubin concentration at the time of evalua- Current experience suggests that combined tion had the shortest duration of survival.27 liver and small bowel transplantation may Arch Dis Child: first published as 10.1136/adc.72.5.447 on 1 May 1995. Downloaded from Thus it is important to refer children for small reduce the chances of intestinal rejection post- bowel transplantation as soon as hepatic dys- operatively.7 It is possible that patients with function becomes apparent or there are diffi- early liver disease may have progression of culties with vascular access in order to allow TPN cholestasis postoperatively particularly if sufficient time for assessment and obtaining a there are problems with establishing intestinal donor. function28 and thus the liver should be replaced if significantly affected. It is important to ensure that complications Assessment related to either liver or intestinal failure are The assessment for small bowel transplanta- medically managed and sepsis is effectively tion focuses on establishing: (1) hepatic and treated. It is our practice to start selective bowel intestinal function; (2) patent vessels; and (3) decontamination (polymyxin B, gentamicin, physical and psychological preparation of child and amphotericin administered orally) once and family. children are placed on the waiting list.

GASTROINTESTINAL FUNCTION Donor procurement and operative It is necessary to establish that intestinal failure technique is irreversible. The precise anatomy, motility, Donor procurement and operative technique and function of the remaining gastrointestinal are now well established.29 30 tract should be assessed. Gastric emptying Grafts must be ABO blood group com- studies and upper and lower gastrointestinal patible and preferably matched for including histology of the bowel cytomegalovirus status. Selection of donor size should be performed. The capacity of the peri- is of critical importance as previous surgery in toneal cavity should be measured as this may the recipient often leads to extensive adhesions be a limiting factor in donor selection. and contraction of the peritoneal cavity so that the ideal donor should weigh approximately 20% less than the recipient. For isolated small HEPATIC FUNCTION bowel transplantation the entire small bowel It is important to assess the extent of together with the right colon is removed with fibrosis/cirrhosis and , its vascular pedicle comprising the superior especially in patients without overt liver mesenteric artery and origin of the portal vein disease. (fig 1). Recent experience has demonstrated reasons vascular to in the colon with For technical the supply advantages including right http://adc.bmj.com/ the liver needs to be determined by ultrasonic the small bowel in terms of fluid and short radiology. The presence or absence of gall chain fatty acid absorption. In combined grafts stones and common stones should be the same bowel is removed but the portal vein established by ultrasound or endoscopic retro- is left in continuity with the liver (fig 2). In grade cholangiopancreatography. both situations the organs are perfused with University of Wisconsin Solution which will allow preservation for up to 10 hours. VASCULAR ACCESS In isolated small bowel grafts the superior on October 4, 2021 by guest. Protected copyright. The presence of patent vessels and vascular mesenteric artery is anastomosed to the aorta, thrombosis is usually established using usually via a conduit of donor iliac artery, and Doppler ultrasound, although angiography venous drainage established by anastomosing may be required. the donor portal vein to the side of the recipi- ent portal vein. The upper end of the graft is

GENERAL ASSESSMENT Anthropometry to measure nutritional status and careful cardiac and pulmonary assessment Superior mesenc t vpin ! tI/sSuperior mesenteric to establish incidence of pulmonary embolism from central venous lines23 is essential.

PSYCHOLOGICAL ASSESSMENT As small bowel transplantation remains a new procedure in the UK it is important that the family are honestly appraised of the risks and complications of this procedure in order to make an informed decision. The psychological preparation of the child is paramount and should include preparation for a stoma and Figure 1 Isolated small bowel transplantation. The donor isolated small bowel is removed with the right colon. The . superior mesenteric artery is anastomosed to the recipient On completion of the assessment, the deci- aorta and the superior mesenteric vein anastomosed to the sion will be made whether the child requires an side of the recipient portal vein. The future ofsmall bowel transplantation 449

Upper IVC. (1) IMMUNOSUPPRESSION AND REJECTION Donor lymphocytes, mesenteric lymph nodes and Peyer's patches are transplanted with the small bowel graft which are replaced in time by Arch Dis Child: first published as 10.1136/adc.72.5.447 on 1 May 1995. Downloaded from Common hepatic recipient lymphocytes leading to either GVHD and superior mesenteric or rejection.32 arteries on aortic Although animal studies suggested that patch GVHD would be a major problem after small Portal bowel transplantation, in practice it has not vein been a significant problem in humans except in immunodeficient patients.26 32 Although combined liver/intestinal trans- plantation has been performed successfully using cyclosporin and steroids,7 33 it is clear Figure 2 Combined small bowel and liver transplantation. that the frequency and severity of both hepatic The donor liver is removed with the small bowel and right and intestinal rejection is much reduced using colon. The venae cavae above and below the liver are FK506, even in recipients of isolated small anastomosed to the recipient cavae; vascular inflow is provided by anastomosing the common hepatic and superior bowel transplantation.34 35 mesenteric arteries to the aorta using an interposition iliac Intestinal rejection may occur from the graft. For clarity the common bile duct has been omitted - seventh postoperative day. The clinical symp- this is anastomosed to the recipient bile duct ifsuitable, or to a Roux-en-Y loop ofeither host or donorjejunum. toms include fever, malaise, abdominal pain, nausea, and an increase in stoma output. Occasionally acute rejection may present with anastomosed to the duodenojejunal flexure. septic shock due to bacterial translocation. The management of the distal intestine varies Confirmation of rejection may be obtained by with individual cases. The transplanted right visualisation of the stoma, or by ileoscopy or colon is anastomosed if possible to the distal endoscopic visualisation of the . The colon in the recipient but a distal ileostomy is intestinal mucosa and stoma may look oede- established proximal to this in all cases to matous, friable, or ulcerated but both clinical facilitate monitoring ofgraft function including manifestations and endoscopic appearances to detect rejection. This is closed may be normal in early rejection. Rejection approximately six months later. may be patchy and multiple endoscopic For combined small bowel liver grafts the are therefore necessary. The histo- presence of cirrhosis with portal hypertension logical signs of rejection which occur include can lead to significant bleeding and great care an inflammatory infiltrate with lymphoblasts, is taken to obtain haemostasis. The liver and eosinophils and macrophages, epithelial necro- small bowel are implanted as a monobloc in sis with crypt cell damage and apoptosis and the orthotopic position. The caval anasto- ulceration and mucosal The sloughing. early http://adc.bmj.com/ moses above and below the liver are per- diagnosis of acute rejection is unsatisfactory formed first. If the recipient cava has been despite attempts to use immunohistochemistry retained, a single anastomosis between the to identify pericryptic CD3 + cells and the donor cava and recipient hepatic veins (piggy appearance of HLA-DR antigens.36 Improved back technique) may be used. The whole graft diagnosis of rejection would be a significant is then revascularised by anastomosing both advance for the future. the hepatic artery and superior mesenteric Continued acute rejection may lead to artery together on a patch to the recipient chronic changes with villous blunting and on October 4, 2021 by guest. Protected copyright. aorta. In this situation the main portal flow to fibrosis of the lamina propria. Rejection occurs the liver comes via the grafted small bowel, in 66% of patients after intestinal transplanta- though the recipient portal vein draining tion and is normally treated by increasing spleen, , , and any residual immunosuppression either with a pulse dose of intestine will need to be anastomosed to the methylprednisolone or increasing FK506. As side of the donor portal vein. The bile duct is rejection is likely to be associated with bacterial anastomosed to either the recipient bile duct translocation it is usual to treat with intra- or to a Roux-en-Y loop. In both situations venous antibiotics and bowel decontamination a feeding is performed so that until the rejection episode has resolved. early postoperative enteral feeding may be Chronic rejection leads to an obliterative given. vasculitis leading to ischaemia and fibrosis of the intestine and its mesentery. It is not nor- mally diagnosed until the graft has been Postoperative management removed and may result in late graft loss. The key to successful postoperative manage- ment is effective teamwork between anaes- thetists, surgeons, paediatricians, nursing and (2) INFECTION paramedical staff. Patients receiving combined Over 90% of children in Pittsburg experienced liver and small bowel transplantation are likely bacterial, viral, or fungal infection despite ade- to spend longer in both the intensive care unit quate prophylaxis.37 Viral infections, especially and in hospital than those receiving isolated cytomegalovirus and Epstein-Barr virus are a small bowel transplantation alone.3' The main particular problem as most children are issues in postoperative management are as negative for these viruses before transplant and follows: selection of potential donors for their 450 Kelly, Buckels

cytomegalovirus and Epstein-Barr virus status 32 ofwhom were children (mean age 3-8 years). is impractical. They performed isolated small bowel transplan- Eleven per cent of children who were tation in 22, combined intestinal/liver grafts in negative for Epstein-Barr virus on FK506 26, and multivisceral (liver, small bowel, Arch Dis Child: first published as 10.1136/adc.72.5.447 on 1 May 1995. Downloaded from developed lymphoproliferative disease, half of stomach, and pancreas) transplants in 11. One whom developed lymphoma.38 The high inci- year patient survival in paediatric recipients was dence of lymphoproliferative disease in 75-6% while graft survival was 68%.10 children on FK50639 is particularly worrying Two year survival figures for the whole and raises important issues about long term group were 80% for isolated small bowel and outcome and survival in this vulnerable group 59% for combined grafts.46 There were 21 of children.38 deaths in the whole group: two operative deaths, seven patients died of rejection, five of sepsis, four of lymphoproliferative disease, two (3) INTESTINAL FUNCTION from respiratory problems, and one of catheter The transplanted intestine undergoes a related problems. number of physiological readjustments before The major complications were bacterial, intestinal function resumes. There is perma- viral or fungal sepsis (90%), acute rejection nent disruption of the extrinsic autonomic (66%), lymphoproliferative disease (6% of all nervous system but only temporary loss of patients and 1 1% of paediatric patients). Nine lymphatic drainage. Mucosal damage sec- patients required intestinal retransplanta- ondary to ischaemia or handling of the donor tion. 10 46 graft recovers within 2-5 days as does intesti- nal motility.40 Animal studies indicate that monosaccharides and disaccharides are equally QUALITY OF LIFE well absorbed and are sensitive markers of the The main aim ofintestinal transplantation is to return of intestinal function.40 restore intestinal function and normal quality Early enteral feeding with a whole protein of life. In the Pittsburg group, 31/39 survivors feed is desirable as both animal and human were totally free from TPN and were on studies suggest that this is associated with less normal oral diets, 5/39 required partial TPN, bacterial translocation and improvement in and one required total TPN.46 mucosal atrophy.4' 42 Carbohydrates are intro- There are potential problems in establishing duced as glucose polymer and the energy normal enteral feeding in children as many density is increased with sucrose and lactose as paediatric patients will have had no previous function improves.43 Fat should be introduced experience of normal feeding. Of 15 paediatric as medium chain triglycerides until lymphatic survivors in the Pittsburg programme six drainage has been re-established, which may children were identified as having significant take several months.40 43 behavioural or functional problems requiring

Motility disturbances secondary to disrup- intensive intervention. Nine children eventu- http://adc.bmj.com/ tion in the enteric nervous system may result in ally attained satisfactory eating habits with delayed gastric emptying or diarrhoea sec- support but five still require supplemental ondary to rapid intestinal transit. The latter enteral feeding.47 may be treated by adding pectin to the feed or The median duration of hospitalisation was with loperamide.43 80 days (range 33-319 days)3' but many patients have required readmission for treat- ment ofrejection and opportunistic infection.37 (4) ASSESSMENT OF SMALL BOWEL FUNCTION on October 4, 2021 by guest. Protected copyright. Intestinal permeability or absorption may be evaluated by urinary excretion of oral 51- Demand for liver and bowel transplanta- chromium EDTA; or D-xylose absorption. In tion in Britain practice, intestinal function is best evaluated The home TPN register held by Professor by measuring the stoma output and assessing Miles Irving at Hope Hospital, Salford, esti- reducing substances and steatocrit.43 mates that approximately 50 adults and children at any one time are receiving long term TPN.14 Approximately 500/o ofthis group Results ofsmall boweliver will recover gut function and TPN will be dis- transplantation continued. Ofthe remaining 25 patients 10 per SURVIVAL year are likely to require small bowel transplan- The first successful recipient of a combined tation.14 Based on our experience in children liver and small bowel transplant has survived with intestinal failure in the West Midlands, we more than four years.44 The London, Ontario estimate 10 children in the UK will need this group have reported three deaths and one graft operation annually (Professor I W Booth, loss in eight adult intestinal recipients44 while personal communication). To date we have the Omaha, Nebraska group report six out of assessed 17 children in Britain for this opera- seven children surviving combined liver and tion.27 small bowel transplantation. One child lost her graft, the remaining children discontinued TPN within 13 weeks postoperatively.45 Conclusion The greatest experience is from the Small bowel and/or liver transplantation is an University of Pittsburg where intestinal trans- established technique with clearly defined plantation has been performed in 59 patients, indications for which there is an appreciable Thefuture ofsmall bowel transplantation 451

15 De-Potter S, Goulet 0, Lamor M, et al. 263 patient years of demand in the UK.27 As experience with this home parenteral nutrition in children. Transplant Proc technique grows it is likely that the indications 1992; 24: 1056-7. 16 Puntis JWL, Holden CE, Snorman S, Finkel Y, George for both combined and isolated small bowel a factor in

RH, Booth IW. Staff training: key reducing Arch Dis Child: first published as 10.1136/adc.72.5.447 on 1 May 1995. Downloaded from transplantation will increase in the future. intravascular catheter sepsis. Arch Dis Child 1991; 66: 335-7. It is clear that GVHD is uncommon in 17 Galaem H, Holliday H, Carachi R, et al. Short bowel humans and that intestinal rejection may be syndrome a collective review. J Pediatr Surg 1992; 27: 592-6. controlled with FK506. Nevertheless before 18 Weber TR, Tracy T, Connors RH. Short bowel syndrome this technique becomes generally accepted, in children; quality of life in an era of improved survival. Arch Surg 1991; 126: 841-6. there are a number of unresolved issues. (1) 19 Wesley JR. Efficacy and safety of total parenteral nutrition There are particular difficulties in finding suit- in paediatric patients. Mayo Clin Proc 1992; 67: 671-5. 20 Bisset WM, Stapleford P, Long S, et al. Home parenteral able donors for small children and unless there nutrition in chronic intestinal failure. Arch Dis Child 1992; are major changes in our donor philosophy, 67: 109-14. never to from 21 Burnes JU, O'Keefe SJ, Flemming CR, et al. Home par- many children will be able benefit enteral nutrition. 3-year analysis of clinical and laboratory this technique, particularly, if referred late with monitoring. journal of Parenteral and Enteral Nutrition are 1992; 16: 327-32. advanced liver disease. (2) There major 22 Ricour C, Gorski AM, Goulet 0, et al. Home parenteral problems with the management of immuno- nutrition in children. Eight years experience with 112 and patients. Clinical Nutrition 1990; 9: 65-71. suppression of the transplanted gut, the 23 Pollard AJ, Sreeram N, Wright JG, Beath SV, Booth IW, prevention and diagnosis of rejection. If this Kelly DA. Pulmonary embolism in children - another will be nec- hazard of parenteral feeding. Gut 1994; 35: S33. technique is to succeed long term it 24 Ingham-Clarke C. Recent progress in intestinal transplanta- essary to establish the correct balance between tion. Arch Dis Child 1992; 67: 976-9. 25 Stera DM, Brett S, Harris K, et al. Participation of endothe- immunosuppression, infection, and rejection. lial cells in the protein C-protein S anticoagulant pathway; (3) In children there may be particular prob- the synthesis and release of protein S. J Cell Biol 1986; lems with the development of normal feeding 102: 1971-8. 26 Tzakis AJ, Todo S, Reyes J. Clinical intestinal transplanta- behaviour and their long term prognosis will be tion; focus on complications. Transplant Proc 1992; 24: risk of 1238-40. affected by the high lymphoproliferative 27 Beath SV, McKiernan PJ, Murphy MS, et al. Paediatric disease in those children who are negative for referrals for combined small bowel and liver transplanta- virus before transplantation. tion: timing and indications; room for improvement? Proc Epstein-Barr Nutr Soc 1994; 54: 2. Future programmes will not only need to 28 Colom G, Goulet 0, Reillon Y, et al. Cholestatic liver answer these questions, but to prospectively disease after small bowel transplantation failure in child- ren. Transplant Proc 1994; 26: 1429-30. evaluate the many social and psychological 29 Todo S, Tzakis A, Abu-Elmagd K, et al. Intestinal trans- to long plantation in composite visceral grafts or alone. Ann Surg issues with reference quality of life, 1992; 216: 223-34. term graft function, and the prevention oflym- 30 Tzakis AG, Todo S, Reyes J, et al. Piggy back orthotopic It will be intestinal transplantation. Surg Gynecol Obstet 1993; 176: phoproliferative disease. also import- 297-8. ant to establish the cost effectiveness ratio of 31 Funovits M, Millar SR, Kovalak J, et al. Hospitalisation and this treatment with funded readmission of intestinal transplantation recipients. compared currently Transplant Proc 1994; 26: 1419-20. health care intervention. 32 Iwaki Y, Starzl TE, Yagihashi A, et al. Replacement of We feel that there is a definite donor lymphoid tissue in small bowel transplants. Lancet already 1991; 337: 818-9.

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