Surgical Management of Short Bowel Syndrome
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1 529446PENXXX / Journal of Parenteral and Enteral NutritionIyer research-article2014 Invited Review Surgical Management of Short Bowel Syndrome Kishore R. Iyer, MBBS, FRCS, FACS 1 Journal of Parenteral and Enteral Nutrition Volume 38 Supplement 1 May S 59S 2014 American Society for Parenteral and Enteral Nutrition DOI: / jpen.sagepub.com hosted at online.sagepub.com Abstract For patients with short bowel syndrome (SBS), surgery can play an important role in preventing, mitigating, and, in some cases, reversing intestinal failure (IF). During intestinal resection, bowel length should be conserved to the fullest extent possible to avoid dependence on parenteral nutrition (PN). Bowel salvage may be improved by initially preserving tissue of questionable viability and later reevaluating during second-look procedures. Once the patient is stabilized, ostomy reversal and recruitment of distal unused bowel should be prioritized whenever feasible. Following progression to IF, surgical management of SBS depends on the symptoms and anatomical characteristics of the individual patient. For carefully selected patients with rapid intestinal transit and dilated bowel, longitudinal intestinal lengthening and tailoring (LILT) and serial transverse enteroplasty (STEP) procedures may provide benefit. Outcomes following STEP and LILT are generally similar, and the choice between these procedures may rest on surgeon preference. For patients with rapid intestinal transit in the absence of bowel dilation, segmental reversal of the small bowel may reduce PN requirements. Intestinal transplantation is the standard of care for patients in whom intestinal rehabilitation attempts have failed and who are at risk of life-threatening complications of PN. Because patients awaiting isolated intestine transplant show increased survival compared with patients awaiting combined intestineliver transplant, early referral of appropriate patients, before the development of advanced liver disease, is critical to enhancing patient outcomes. (JPEN J Parenter Enteral Nutr. 2014;38(suppl 1):53S-59S) Keywords short bowel syndrome; intestinal failure; surgery; intestinal transplant A useful surgical definition for short bowel syndrome (SBS) relates to the functional aspect of intestinal failure (IF) that is, failure of the intestine to adequately meet the body s requirements for fluid, macronutrients, and micronutrients. Such a definition moves away from specific reference to residual bowel length and includes functional forms of IF, such as pseudo-obstruction, in which residual bowel may be normal in length but operationally deficient. Notwithstanding the above, effective surgical management of IF requires an accurate understanding of disease origin, remnant bowel length, and other residual anatomic characteristics, such as presence of stomas, blind loops, or colonic remnant. This information is best obtained from a careful review of the patient s history, including prior surgical notes, direct conversation with previous surgeons when possible, and review of available imaging. Armed with this historical context, the surgeon can tailor individualized surgical management for patients dependent on parenteral nutrition (PN). The surgeon should be viewed as a key stakeholder in partnership with a gastroenterologist and/or nutrition support clinician in the care of patients with IF. Such multidisciplinary management, reviewed by Matarese et al, 1 allows for optimal planning in terms of deployment of different treatment options, evaluation of therapeutic success, and determination of timing for escalated intervention, whether it be surgery or even intestinal transplantation. It is also important that one key stakeholder in the multidisciplinary team take ownership of long-term vascular access maintenance for each patient. That function is often best managed by the team surgeon, often in close partnership with the interventional radiologist. The Role of Surgery in Preventing Intestinal Failure The role of surgery in IF often begins with the prevention of IF. Although available supporting data are limited, early recognition of patients at high risk for loss of critical bowel length From the 1 Adult and Pediatric Intestinal Transplant & Rehabilitation Program, Mount Sinai Medical Center, New York, New York. Financial disclosure: The publication of the supplement in which this article appears is supported by an educational grant from NPS Pharmaceuticals, Inc (Bedminster, NJ). K.R.I. has served as a site investigator, advisory board member, and consultant for NPS Pharmaceuticals, Inc. No financial compensation was provided to K.R.I. for the preparation of this work. Funding for medical writing assistance was provided by NPS Pharmaceuticals, Inc. Received for publication November 15, 2013; accepted for publication March 4, Corresponding Author: Kishore R. Iyer, MBBS, FRCS, FACS, Adult and Pediatric Intestinal Transplant & Rehabilitation Program, Mount Sinai Medical Center, One Gustave L. Levy Place Box 1104, New York, NY 10029, USA. Kishore.Iyer@mountsinai.org
2 54S Journal of Parenteral and Enteral Nutrition 38(Suppl 1) Table 1. Options for Surgical Management of Short Bowel Syndrome. Operations to Correct Slow Transit Operations to Improve Intestinal Motility With Dilated Bowel Operations to Slow Intestinal Transit in the Absence of Bowel Dilatation Operations to Increase Mucosal Surface Area Consider the possibility of strictures, partial obstructions, blind loops, or enteroenteric fistulas; diagnose and treat accordingly Creation of valves a Tapering enteroplasty Longitudinal intestinal lengthening and tailoring (Bianchi LILT procedure) Serial transverse enteroplasty (STEP) Intestinal plication b Segmental reversal of the small bowel (SRSB) Isoperistaltic colonic interposition Sequential intestinal lengthening Controlled tissue expansion a Of historical interest only; not currently recommended because of disproportionate risk of adverse events. b Of historical interest only; not currently recommended because of inefficacy. should trigger conservative strategies to avoid preventable bowel loss, thereby potentially improving outcomes. 2 It is critical in such cases to initially preserve bowel of questionable viability and later reevaluate during planned second-look operations. 3 Our own adoption of the clip and drop-back technique described by Grosfeld and his group (Vaughan et al 4 ) has yielded excellent results and allowed us to improve bowel salvage in difficult cases. Critically ill patients should be monitored for risk of abdominal compartment syndrome (ACS) to prevent additional bowel loss. 5 Attempts to achieve abdominal closure may be better delayed until the patient is stabilized. The risk of ACS can be minimized by the liberal use of temporary mesh closure to manage bowel swelling following periods of ischemia reperfusion. 6 Used together, these strategies allow us to avoid stomas in most cases of impending IF, which usually conserves bowel length and poses no obvious short-term disadvantages. In the context of preventing IF, it is worth reiterating the positive role of strictureplasties and conservative surgical strategies in the long-term surgical management of patients with Crohn s disease. 7-9 Following the acute phase, once the patient is adequately resuscitated, the surgical priority becomes the planned takedown of stomas and recruitment of distal unused bowel. Although somewhat routine, ostomy reversal may be the single most useful intervention that a surgeon can undertake in the management of IF. This provides the absorptive benefits of recruiting all available bowel, and patients without high-output stomas may have fewer catheter-related infections, although data to support this observation are lacking. 10 The role of the colon in generating additional energy through the bacterial breakdown of complex carbohydrates to short-chain fatty acids is well recognized and provides additional justification for the avoidance of stomas wherever technically possible In rare cases of ultrashort bowel with intact colon, in which bile acid mediated diarrhea has proven unmanageable and disabling, we have elected to convert a high jejunostomy to a sigmoid colostomy with recruitment of most of the colon. This tactic achieves appreciable benefit while addressing quality-of-life issues. Definitive Surgical Management of Intestinal Failure Surgical options in patients with long-term IF fall into 4 main categories: operations to (1) correct slow transit, (2) improve intestinal motility in cases of dilated bowel, (3) slow intestinal transit in the absence of bowel dilatation, and (4) increase mucosal surface area (Table 1). Operations to Correct Slow Transit Slow transit in SBS is relatively rare and should trigger a search for strictures, partial obstructions or blind loops, and enteroenteric fistulas. 15 These are often sequelae of the underlying disease leading to SBS, such as Crohn s disease, and often require meticulous investigation to diagnose and treat appropriately. 16 A high index of suspicion regarding patients whose clinical behavior is at odds with their underlying anatomical characteristics should permit the discovery and satisfactory resolution of such cases. Operations to Improve Intestinal Motility in Cases of Dilated Bowel Rapid intestinal transit is a nearly universal clinical challenge in SBS and should elicit prompt investigation into underlying structural causes. Segmental bowel dilatation with poor peristalsis is a frequent finding in patients with SBS and rapid transit, and it often results in clinical features of small bowel bacterial overgrowth In our experience, small intestinal bacterial overgrowth against a background of structural bowel abnormality is often refractory to conventional medical treatment and requires surgical correction of the underlying cause. Excessive intestinal dilatation is most easily managed by a simple tapering enteroplasty, in which a strip of intestine along the antimesenteric border of dilated bowel is removed using a mechanical stapling device. 20 This procedure is most applicable when bowel length is considered adequate and when loss of surface area is an acceptable tradeoff for better prograde peristalsis.
3 Iyer Figure 1. The longitudinal intestinal lengthening and tailoring (LILT) procedure, originally described by Bianchi. 21 (A) Creation of the avascular space along the mesenteric border of a dilated loop of bowel; (B) view of avascular space; (C) splitting of the bowel lengthwise; (D) view of newly created hemi-loops; (E) isoperistaltic anastomosis of hemi-loops. Reproduced with permission from Bianchi A. Intestinal loop lengthening a technique for increasing small intestinal length. J Pediatr Surg. 1980;15(2):147. In cases where bowel length is critical, the longitudinal intestinal lengthening and tailoring (LILT) operation first described by Adrian Bianchi 21 accomplishes intestinal tapering without loss of surface area. In the LILT procedure, an avascular space is created longitudinally along the mesenteric border of a dilated loop of bowel. The bowel is then split lengthwise, taking care to allocate alternating blood vessels to each side. Each side of the split bowel is then tubularized, generating 2 hemi-loops that are anastomosed end to end in isoperistaltic fashion (Figure 1). When completed, LILT creates a loop of bowel that is twice the length of the original and half the original diameter; no new bowel is created. The decrease in bowel diameter accomplished without loss of surface area is likely more important than the gain in length. Bianchi s early personal experience with the procedure in 20 children resulted in 7 of 9 survivors attaining enteral autonomy from PN at a mean follow-up of 6.4 years. 22 We concur with Bianchi s opinion that LILT should be applied with extreme caution in patients 55S with ultrashort bowel and in the presence of liver disease. 22,23 However, notwithstanding the need for cautious patient selection, we have reported on functional liver recovery even in the presence of moderate to advanced liver disease in carefully chosen patients following autologous gut salvage. 24 Based on a recent report, outcomes following autologous gastrointestinal reconstruction are improving with accumulating experience. Of 27 children undergoing various autologous procedures for SBS, including 19 LILT procedures, overall survival was 92%, and >90% of survivors achieved independence from PN. 25 Tapering without loss of surface area is accomplished effectively and relatively simply by the serial transverse enteroplasty (STEP) procedure described by Kim et al 26 in In the STEP procedure, the luminal channel is narrowed by firing a series of staples perpendicular to the long axis of the bowel in a zig-zag pattern without interfering with the blood supply of the bowel (Figure 2). In a long-term study of 12 pediatric patients who underwent STEP, 8 (67%) patients remained alive and transplant-free at a median follow-up of 5.7 years. Of those 8 patients, 7 achieved independence from PN. In addition, the dilated segment showed an 87% increase in median length and a 67% decrease in mean internal diameter. 27 The choice of lengthening procedure between the Bianchi LILT and the technically simpler STEP remains somewhat unclear and until recently seemed related to surgeon preference. In a retrospective, uncontrolled, single-center study, Sudan et al 28 reported outcomes of 64 patients who underwent a total of 43 LILT and 34 STEP procedures over a 24-year period. Overall survival was 91% at a median follow-up of 3.8 years. Enteral autonomy was achieved by 69% of PN-dependent patients, and liver disease was reversed in >80% of affected patients. Differences between the 2 procedures were small, although nonsignificant trends were documented for a lower rate of weaning from PN, longer time to PN discontinuation, and a higher incidence of complications requiring reoperation after LILT than after the STEP procedure. Of note in this series, 14% of patients underwent intestinal transplantation at a median of 2.9 years. Transplantation was required more often following LILT than after the STEP procedure (18.6% vs 5%, respectively; P =.03), although this difference may be due in part to the longer follow-up time for patients receiving LILT (5.9 vs 1.7 years for STEP). 28 A recent retrospective observational study of 111 consecutive patients enrolled in the international STEP registry provides additional impetus for more serious consideration of the appropriateness of the STEP procedure in suitable patients. 29 Of 97 patients for whom complete data were available, 11 patients died and 5 required intestinal transplantation. In a multivariate analysis, risk of progression to transplantation or death was greater among patients with shorter bowel length before surgery and higher conjugated bilirubin levels. Of 78 PN-dependent patients older than 7 days at the time of STEP, only 47% of patients achieved full enteral autonomy at a median of 21 months. 29 More recent data suggest improved
4 56S Journal of Parenteral and Enteral Nutrition 38(Suppl 1) Figure 2. In the serial transverse enteroplasty (STEP) procedure, staples are fired perpendicular to the long axis of the bowel in a zigzag pattern to make and close incisions and thereby reduce lumen diameter and lengthen the bowel. The (A) first and (B) second staples are placed; (C) with the appropriate placement of multiple staples, the bowel is extended and tapered. Reproduced with permission from Kim et al. Serial transverse enteroplasty (STEP): a novel bowel lengthening procedure. J Pediatr Surg. 2003;38(3):426. long-term outcomes following the LILT compared with the STEP procedure, with special reference to overall survival, autonomy from PN, and avoidance of intestinal transplantation. The more general applicability of the technically simpler STEP procedure and a trend to the LILT procedure being performed at centers with special expertise in the management of SBS overall may be important confounding variables. Operations to Slow Intestinal Transit in the Absence of Bowel Dilatation Of procedures designed to slow transit in the absence of bowel dilatation, segmental reversal of the small bowel (SRSB) shows the greatest promise. 30 SRSB creates an antiperistaltic segment of bowel approximately cm in length, located ~10 cm proximal to an end-stoma or the small bowel-colon anastomosis. 10,31 Of 38 patients undergoing SRSB over a 25-year period at a single center, 17 (45%) achieved complete independence from PN. Among patients who were not weaned, PN requirements were decreased by a median 3 days per week. A shorter interval between enterectomy and SRSB, an SRSB >10 cm, and an extended stay with the nutrition unit were significantly associated with enteral autonomy. 32 Isoperistaltic colonic interposition, the relocation of a segment of colon to the small intestines while maintaining peristaltic directionality, has seen limited use following the initial description of the procedure in puppies by Hutcher and Salzberg in The largest available study included 6 infants who were followed for months. Three patients achieved enteral autonomy from PN within 4 months of surgery. The remaining 3 patients were not weaned from PN, and all died, at an average of 20 months postsurgery. 34 Renewed interest in its application in infants with extreme SBS (A. Morabito, personal communication, 2012) should be considered with caution, given the improving outcomes seen with intestinal transplantation. Operations to Increase Mucosal Surface Area Although the creation of neomucosa remains an elusive goal, use of sequential lengthening procedures and controlled tissue
5 Iyer expansion (CTE) before bowel lengthening may have immediate, albeit limited, clinical application. 35,36 The theoretical basis for the strategy of CTE of nondilated bowel in preparation for definitive intestinal lengthening was laid out in experimental work on pigs by the demonstration of mucosal hypertrophy and gain in length and diameter of partially obstructed intestine. 37 The Manchester experience with CTE, limited to only 10 cases, is nevertheless noteworthy for having reached the goal of performing LILT procedures in all 10 patients and, more important, for accomplishing enteral autonomy in 9 of the 10 patients. Despite the fact that this is a limited, uncontrolled retrospective series, lacking important anatomical details such as presence or absence of colon, the long-term results are impressive and this approach merits further study. A more immediate application of these principles is the demonstration of feasibility of repeat intestinal lengthening with the STEP procedure. 38 However, more recent experience from the Ann Arbor group suggests that redilation after prior lengthening may be an overall poor prognostic sign and merits caution. 39 Intestinal Transplantation For patients in whom all attempts at intestinal rehabilitation have failed and who are at risk of life-threatening complications of PN, intestinal transplantation has emerged as the standard of care. The US Centers for Medicare and Medicaid Services (CMS) approved intestinal transplantation for patients with irreversible IF and PN-related complications in 2000 and extended the approval to multivisceral transplantation the following year. The CMS definition of PN failure includes the following: 1. Presence of PN-associated liver disease 2. Loss of central venous access (ie, loss of 3 6 central venous access sites in children or 2 4 central venous access sites in adults) 3. Recurrent catheter-related sepsis or a single episode of fungal sepsis 4. Recurrent bouts of severe dehydration or metabolic abnormalities 40 Contraindications to intestinal transplantation mirror those for the other organs. Active infection and malignancy constitute absolute contraindications to transplant, whereas severe neurodevelopmental disability or psychosocial factors may be considered relative contraindications in some cases. In the absence of liver disease, isolated intestine transplantation, often including the right colon, is the procedure of choice. Advanced liver disease, especially in the presence of significant portal hypertension, mandates combined liverintestine transplant with multivisceral transplantation, including pancreas and stomach for patients with multiorgan disease or complete splanchnic venous thrombosis. For patients with 57S moderate biochemical and histologic liver disease, we have demonstrated that successful isolated intestinal transplantation results in biochemical improvement of liver function and may also allow histologic liver recovery. 41,42 Despite a trend for earlier consideration of intestinal transplantation, >50% of patients listed for intestinal transplantation are simultaneously listed for liver replacement. 43 This is an unfortunate reflection of the serious issue of late referral for intestinal transplantation, which allows PN-associated liver disease to advance to the point where combined liver and intestinal transplantation is mandated. Because of the vagaries of the liver allocation system and the unique clinical characteristics of PN-associated liver disease, patients awaiting combined liver-intestine transplant are at a significant survival disadvantage. The mortality rate on the liver-intestine transplant waiting list can reach 30%, compared with a 9% mortality rate on the isolated intestine transplant list. 44 Thus, early referral of patients who are failing PN may increase the rate of isolated intestinal transplantation and thereby reduce the significant mortality associated with waiting list placement. Until very recently, potential transplant recipients were matched to suitable donors only on the basis of size and blood type. A growing appreciation of the potential for antibodymediated rejection has led to more nuanced matching and the implementation of strategies to desensitize recipients with preformed antibodies. 45,46 Advances in immunosuppression with antibody induction, careful surveillance for opportunistic infections, and overall improvements in nutrition and posttransplant management have led to steadily improving outcomes in intestinal transplantation. 47 Patient and graft survival rates at 1 year are 89% and 79%, respectively, following isolated intestinal transplantation and are 72% and 69%, respectively, following combined liver-intestine transplantation. 43 However, the early survival advantage for isolated intestine recipients appears to be blunted in the longer term, perhaps because of an apparent higher incidence of chronic rejection in this population compared with recipients of combined liver-intestine transplants. 43,48,49 The relative tolerogenic capacity of liver-derived lymphocytes compared with intestine-derived lymphocytes may explain the immunoprotective effects of combined liver-intestinal transplants compared with isolated intestinal transplants. 50 It is hoped that newer strategies to improve human leukocyte antigen matching and to account for the possible role of B lymphocytes in long-term graft survival may allow us to translate improved early outcomes into prolonged gains. Outcomes for patients following intestinal transplantation are now similar to those for patients who are permanently dependent on PN. 51 Furthermore, in comparing outcomes between PN dependence and intestinal transplantation, it is important to appreciate that the majority of patients currently undergoing intestinal transplantation are those for whom continued maintenance on PN is likely to carry a 100% mortality risk even for the medium term. In addition, intestinal
6 58S Journal of Parenteral and Enteral Nutrition 38(Suppl 1) transplantation is the only available therapy for patients with inoperable tumors at the root of the mesentery, such as desmoid tumors. The list of indications for intestinal transplantation is continually growing and may expand to include some quality-of-life reasons. The day may not be far off when intestinal transplantation becomes accepted preemptive therapy for patients with PN dependence that is refractory to medical, nutrition, and conventional surgical therapies, without the need to wait for onset of life-threatening complications. Acknowledgments Medical writing assistance was provided by Heather Heerssen, PhD, of Complete Healthcare Communications, Inc (Chadds Ford, PA) under the direction of the author. K.R.I. is responsible for the content of this manuscript and had final approval of all revisions. References 1. Matarese LE, Jeppesen PB, O Keefe SJD. Short bowel syndrome in adults: the need for an interdisciplinary approach and coordinated care. JPEN J Parenter Enteral Nutr. 2014;38(suppl 1):60S-64S. 2. Thompson JS. Surgical considerations in the short bowel syndrome. Surg Gynecol Obstet. 1993;176: Weber TR, Lewis JE. The role of second-look laparotomy in necrotizing enterocolitis. J Pediatr Surg. 1986;21: Vaughan WG, Grosfeld JL, West K, Scherer LR III, Villamizar E, Rescorla FJ. Avoidance of stomas and delayed anastomosis for bowel necrosis: the clip and drop-back technique. J Pediatr Surg. 1996;31: An G, West MA. Abdominal compartment syndrome: a concise clinical review. Crit Care Med. 2008;36: Fansler RF, Taheri P, Cullinane C, Sabates B, Flint LM. Polypropylene mesh closure of the complicated abdominal wound. Am J Surg. 1995;170: Dietz DW, Fazio VW, Laureti S, et al. Strictureplasty in diffuse Crohn s jejunoileitis: safe and durable. Dis Colon Rectum. 2002;45: Thompson JS, Iyer KR, DiBaise JK, Young RL, Brown CR, Langnas AN. 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JPEN J Parenter Enteral Nutr. 2014;38(suppl 1):14S-22S. 15. Thompson JS. Strategies for preserving intestinal length in the shortbowel syndrome. Dis Colon Rectum. 1987;30: Lu KC, Hunt SR. Surgical management of Crohn s disease. Surg Clin North Am. 2013;93: Adzick NS, Harrison MR, delorimier AA. Tapering duodenoplasty for megaduodenum associated with duodenal atresia. J Pediatr Surg. 1986;21: Thompson J, Sudan D. Intestinal lengthening for short bowel syndrome. Adv Surg. 2008;42: De Lorimier AA, Norman DA, Goodling CA, Preger L. A model for the cinefluoroscopic and manometric study of chronic intestinal obstruction. J Pediatr Surg. 1973;8: Weber TR, Vane DW, Grosfeld JL. Tapering enteroplasty in infants with bowel atresia and short gut. Arch Surg. 1982;117: Bianchi A. Intestinal loop lengthening a technique for increasing small intestinal length. J Pediatr Surg. 1980;15: Bianchi A. Longitudinal intestinal lengthening and tailoring: results in 20 children. J R Soc Med. 1997;90: Bianchi A. From the cradle to enteral autonomy: the role of autologous gastrointestinal reconstruction. Gastroenterology. 2006;130:S138-S Iyer KR, Horslen S, Torres C, Vanderhoof JA, Langnas AN. Functional liver recovery parallels autologous gut salvage in short bowel syndrome. J Pediatr Surg. 2004;39: ; discussion Khalil BA, Ba ath ME, Aziz A, et al. Intestinal rehabilitation and bowel reconstructive surgery: improved outcomes in children with short bowel syndrome. J Pediatr Gastroenterol Nutr. 2012;54: Kim HB, Fauza D, Garza J, Oh JT, Nurko S, Jaksic T. Serial transverse enteroplasty (STEP): a novel bowel lengthening procedure. J Pediatr Surg. 2003;38: Oliveira C, de Silva N, Wales PW. Five-year outcomes after serial transverse enteroplasty in children with short bowel syndrome. J Pediatr Surg. 2012;47: Sudan D, Thompson J, Botha J, et al. Comparison of intestinal lengthening procedures for patients with short bowel syndrome. Ann Surg. 2007;246: ; discussion Jones BA, Hull MA, Potanos KM, et al. Report of 111 consecutive patients enrolled in the International Serial Transverse Enteroplasty (STEP) Data Registry: a retrospective observational study. J Am Coll Surg. 2013;216: Gibson LD, Carter R, Hinshaw DB. Segmental reversal of small intestine after massive bowel resection: successful case with follow-up examination. JAMA. 1962;182: Panis Y, Messing B, Rivet P, et al. Segmental reversal of the small bowel as an alternative to intestinal transplantation in patients with short bowel syndrome. Ann Surg. 1997;225: Beyer-Berjot L, Joly F, Maggiori L, et al. Segmental reversal of the small bowel can end permanent parenteral nutrition dependency: an experience of 38 adults with short bowel syndrome. Ann Surg. 2012;256: ; discussion Hutcher NE, Salzberg AM. Pre-ileal transposition of colon to prevent the development of short bowel syndrome in puppies with 90 percent small intestinal resection. Surgery. 1971;70: Glick PL, de Lorimier AA, Adzick NS, Harrison MR. Colon interposition: an adjuvant operation for short-gut syndrome. J Pediatr Surg. 1984;19: Murphy F, Khalil BA, Gozzini S, King B, Bianchi A, Morabito A. Controlled tissue expansion in the initial management of the short bowel state. World J Surg. 2011;35: Georgeson K, Halpin D, Figueroa R, Vincente Y, Hardin W Jr. Sequential intestinal lengthening procedures for refractory short bowel syndrome. J Pediatr Surg. 1994;29: ; discussion Collins J III, Vicente Y, Georgeson K, Kelly D. Partial intestinal obstruction induces substantial mucosal proliferation in the pig. J Pediatr Surg. 1996;31: Andres AM, Thompson J, Grant W, et al. Repeat surgical bowel lengthening with the STEP procedure. Transplantation. 2008;85: Miyasaka EA, Brown PI, Teitelbaum DH. Redilation of bowel after intestinal lengthening procedures an indicator for poor outcome. J Pediatr Surg. 2011;46: Centers for Medicare & Medicaid Services. National coverage determination (NCD) for intestinal and multi-visceral transplantation (260.5). AAAABAAAAAA&. Accessed August 22, 2013.
7 Iyer 59S 41. Fiel MI, Sauter B, Wu HS, et al. Regression of hepatic fibrosis after intestinal transplantation in total parenteral nutrition liver disease. Clin Gastroenterol Hepatol. 2008;6: Fiel MI, Wu HS, Iyer K, Rodriguez-Laiz G, Schiano TD. Rapid reversal of parenteral-nutrition-associated cirrhosis following isolated intestinal transplantation. J Gastrointest Surg. 2009;13: Mazariegos GV, Steffick DE, Horslen S, et al. Intestine transplantation in the United States, Am J Transplant. 2010;10: Chungfat N, Dixler I, Cohran V, Buchman A, Abecassis M, Fryer J. Impact of parenteral nutrition-associated liver disease on intestinal transplant waitlist dynamics. J Am Coll Surg. 2007;205: Hawksworth JS, Rosen-Bronson S, Island E, et al. Successful isolated intestinal transplantation in sensitized recipients with the use of virtual crossmatching. Am J Transplant. 2012;12(suppl 4):S33-S Gondolesi G, Blondeau B, Maurette R, et al. Pretransplant immunomodulation of highly sensitized small bowel transplant candidates with intravenous immune globulin. Transplantation. 2006;81: Fishbein TM. Intestinal transplantation. N Engl J Med. 2009;361: Parizhskaya M, Redondo C, Demetris A, et al. Chronic rejection of small bowel grafts: pediatric and adult study of risk factors and morphologic progression. Pediatr Dev Pathol. 2003;6: Abu-Elmagd KM, Costa G, Bond GJ, et al. Five hundred intestinal and multivisceral transplantations at a single center: major advances with new challenges. Ann Surg. 2009;250: Murase N, Starzl TE, Tanabe M, et al. Variable chimerism, graft-versus-host disease, and tolerance after different kinds of cell and whole organ transplantation from Lewis to brown Norway rats. Transplantation. 1995;60: Sudan DL. Treatment of intestinal failure: intestinal transplantation. Nat Clin Pract Gastroenterol Hepatol. 2007;4:
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