© 2013 John Wiley & Sons A/S.

Clin Transplant 2013: 27 (Suppl. 25): 56–65 DOI: 10.1111/ctr.12190

Intestinal transplantation: review of operative techniques Nickkholgh A, Contin P, Abu-Elmagd K, Golriz M, Gotthardt D, Morath C, Schemmer P, Mehrabi A. Intestinal transplantation: review of operative techniques. Abstract: The improvement of outcomes in intestinal transplantation (ITx) over the last two decades has been made possible through standardization in surgical techniques, improvements in immunosuppressive and induction protocols, and post-operative patient care. From a surgical technical point of view, all different types of small bowel containing transplants can be categorized into three main prototypes, including isolated small bowel, liver–small bowel, and multivisceral transplantations. In this review, we describe these three main prototypes and discuss the most important technical modifications of each type, as well as donor and recipient procedures, and highlight the more recent operative technical topics of discussion in the literature.

Arash Nickkholgha, Pietro Contina, Kareem Abu-Elmagdb, Mohammad Golriza, Daniel Gotthardtc, Christian Morathc, Peter Schemmera and Arianeb Mehrabia a

Department of General, Visceral and Transplantation Surgery, Ruprecht-Karls University, Heidelberg, Germany, bTransplant Center, Center for Gut Rehabilitation & Transplantation (CGRT), The Cleveland Clinic Foundation, Cleveland, OH, USA and c Department of Internal Medicine, RuprechtKarls University, Heidelberg, Germany Key words: donor – intestinal transplantation – multivisceral – organ procurement – recipient – small bowel – techniques Corresponding author: Arianeb Mehrabi, MD, Department of General, Visceral and Transplantation Surgery, Ruprecht-Karls University, INF 110, 69120 Heidelberg, Germany. Tel.: +49(0) 6221/56 6111; fax: +49(0) 6221/56 7470; e-mail: [email protected]. de Conflict of interest: None. Accepted for publication 12 June 2013

The animal experimental studies regarding intestinal transplantation (ITx) trace back to innovative works of Alexis Carrel a century ago (1), and later in the middle of the twentieth century by Lillehei et al. (2) as an isolated graft, and subsequently by Starzl and Kaupp (3) as part of a multivisceral “mass homotransplantation” in canine model. During the next three decades, several attempts to perform clinical ITx ended up in dismal results, with only a few sporadic successful cases at the end of 1980s including the first successful multivisceral transplant in Pittsburgh, USA, in 1987 (4), followed by the first successful isolated ITx in 1989 in Kiel, Germany (5), and in Paris, France (6), and successful liver-small bowel transplant in Ontario, Canada (7). However, the evolution of the procedure from a highly experimental method with

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unsatisfactory results into an established therapeutic modality with significant increase in patient and graft survival rates was only feasible after the introduction of tacrolimus in clinical ITx in the early 1990s (8). This milestone was fortified with advances in induction protocols, post-transplant care, and operative techniques, followed by the approval of funding of intestinal, liver-intestinal, and multivisceral transplants by the Centers for Medicare and Medicaid Services in the United States a decade later in 2001 (9). From the surgical point of view, all different types of small bowel containing transplants can be categorized into three main forms depending on using the jejunoileal axis alone, that is, “isolated small bowel transplantation,” or adding one or a combination of abdominal organs to small bowel

Operative techniques of intestinal transplantation as a central core, ranging from “liver–small bowel transplantation” to “multivisceral transplantation” (Fig. 1). While isolated small bowel and liver– small bowel transplantation represent exact descriptions, the term “multivisceral transplantation” is used for the transplantation of any small bowel contained visceral allograft which includes “stomach” (10), which can be “full” or “modified” according to the inclusion or exclusion of donor liver, respectively. The decision to select a certain type is based on patient’s underlying disease, age, anatomy, degree of the dysfunction of other abdominal organs, and the transplant center’s discretion. In this review, we first describe the three main prototypes of ITx and reflect the most important technical modifications of each type, donor, and organ procurement techniques, and address special issues in recipient operation, as well as some important technical topics of debate.

Main prototypes of ITx Isolated small bowel transplantation

This type of transplant is the method of choice for patients with intestinal failure with preserved liver function. It has been more frequently used in

adults than children (55% of all adults ITx vs. 37% of all children ITx; 11). This could be partly due to the greater need for a liver–small bowel transplant in children as a result of a higher incidence of end-stage liver disease associated with total parenteral nutrition in this age group. The indications for this type of transplant can be collectively divided into short bowel syndrome, motility disorders, malabsorption syndromes, and gastrointestinal (GI) neoplasm (depending on the extent of disease). In patients with concomitant pancreatic insufficiency and intestinal failure, such as patients with cystic fibrosis, chronic pancreatitis, or type 1 diabetes mellitus, a composite small bowel–pancreas graft vs. simultaneous small bowel–pancreas transplant may be considered (Fig. 2; 12). Liver–small bowel transplantation

The combined liver–small bowel transplantation is usually indicated for patients with intestinal failure who have developed end-stage liver failure due to the long-term parenteral nutrition. Patients with concomitant liver failure and portomesenteric thrombosis may also benefit this procedure. The procedure can be accomplished using a composite allograft (Fig. 3A) vs. organs

Fig. 1. Main prototypes of intestinal transplant. From left to right: isolated small bowel transplantation, liver–small bowel transplantation, and multivisceral transplantation. The modified “liver-sparing” multivisceral graft has been depicted in the inset.

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Nickkholgh et al. Multivisceral transplantation

Full or modified multivisceral transplantation comprises nearly 24% of adult and 13% of pediatric intestinal transplants (17), and is indicated for patients with complex abdominal pathology including massive GI polyposis, traumatic loss of the abdominal viscera, extensive abdominal desmoid tumors, locally aggressive non-metastasizing neoplasms, generalized hollow visceral myopathy/neuropathy, and complete thrombosis of the splanchnic arterial or portal venous system(s) with vascular or hepatic decompensation (18).

Donor techniques Fig. 2. Composite small bowel–pancreas graft. From posterior view. Note the vascular interpositions. The donor splenic artery and superior mesenteric artery are anastomosed to a Y-interposition of donor common iliac artery as the graft arterial stump. Donor common iliac vein may be used as a venous interposition to lengthen the graft portal vein.

implanted separately from the same donor. The composite allograft includes the pancreaticoduodenal axis along with liver and small bowel to keep the hepatoduodenal ligament intact and avoid the biliary reconstruction (13, 14). Pediatric or small candidates requiring combined liver and intestinal transplants may benefit from a composite “reduced-size liver”–small bowel graft, which may consist left, right, or extended right lobes of the liver; the vascular and biliary structures are maintained along with the pancreaticoduodenal axis (Fig. 3B; 15, 16).

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Donor selection

Young hemodynamically stable ABO-compatible brain-dead donors with a BMI ≤ 25 matching with recipient and an intensive care stay ≤5 d with little vasopressor requirement receiving enteral feeding are desirable. Cross-match should be negative and cold ischemia time should remain ≤6 h to prevent irreversible intestinal mucosal injury (19). The use of CMV-positive donors has been approached more liberally during the last decade (20). Donor procedures

The organ procurement procedure can be divided into three main sequences: organ dissection with

B

Fig. 3. Liver–small bowel composite graft. (A) Note that the composite graft does not have a portal venous drainage. Liver is anastomosed to the inferior vena cava using the piggyback technique. The arterial “Carrel” patch has been described in recipient techniques. Note that the graft contains donor pancreas, too. (B) Composite “reduced-size liver”–small bowel graft containing the donor left liver lobe.

Operative techniques of intestinal transplantation intact donor circulation, in situ flushing through aortic infusion, and back-table procedure. Organ dissection. The organ dissection starts with the mobilization of the right hemicolon, including the hepatic flexure (Cattell–Braasch maneuver), as well as the mobilization of duodenum along with the head of pancreas to the midline (Kocher maneuver). It is followed by the exposure of abdominal aorta and inferior vena cava (IVC) from bifurcation up to superior mesenteric artery (SMA), and the dissection of gastrocolic ligament and the mobilization of left hemicolon to perform a total colectomy. If the right colon is to be retrieved, the colon transection line will be distal to the shedding area of middle colic artery (MCA) branch of SMA. Subsequently, a medial visceral rotation (the Mattox maneuver) is performed to mobilize the pancreatic tail and spleen. The highest jejunal arcades are then divided close to jejunal wall, and proximal jejunum is transected 5–10 cm distal to Treitz ligament with linear stapler. In case of a composite small bowel–pancreas or composite liver–(pancreas)small bowel procurement, the transection line will be the post-pyloric duodenum. In multivisceral graft procurement, the cardia will be linearly stapled after the division of gastrolienal ligament and dissection of the distal esophagus. The simultaneous procurement of small bowel, pancreas, and liver from the same donor to enhance the organ utility has been described (21). In this case, as the gastroduodenal artery is ligated during the removal of the liver, the pancreas will be deprived of the superior pancreaticoduodenal artery, which is the terminal branch of gastroduodenal artery. Therefore, care should be taken to leave the inferior pancreaticoduodenal artery intact with the pancreas to avoid the devascularization of the pancreatic head and uncinate process. As this branch originates just proximal to the origin of the MCA (and sometimes from the first jejunal branch of the SMA), the risk can be minimized through the ligation of MCA and limiting the dissection level of SMA just below the level of the ligated MCA (and even the first jejunal branch of the SMA). When the SMA is short, for example in case, the donor SMA has to be divided short distal to the origin of an accessory right hepatic artery, the arterial stump can be lengthened using an interposition of the donor common iliac or common carotid arteries. Left gastric artery is ligated (with caution to preserve an aberrant left hepatic branch) and short gastric vessels to the spleen are divided (they are preserved in multivisceral graft procurement). For the purpose of the

composite “reduced-size liver”–small bowel procurement, the splitting of the liver may be performed in situ with an intact circulation as is described elsewhere (22). In composite liver–(pancreas) small bowel as well as multivisceral procurement, a large Carrel patch containing the origin of celiac trunk (CT) and SMA is excised from the ventral aortic wall (see below); it is mandatory to first identify and protect the blood supply of both kidneys. For the purpose of isolated ITx, one has to dissect superior mesenteric vein (SMV) for the venous drainage. In situ flushing. After the dissection of liver and thoracic organs, and systemic administration of heparin, the abdominal aorta is cross-clamped below the diaphragmatic crura and IVC is closed proximal to the bifurcation, and in situ flushing with either the University of Wisconsin (UW) or histidine-tryptophan-ketoglutarate solution (HTK) is started. Perfusion of the intestine is limited to about 500–1000 mL by manual compression of the SMA to avoid hypoperfusion (23). After the completion of the in situ flushing, the graft procurement will be completed. New clinical data of a retrospective cohort suggest no significant difference in terms of graft and patient survival at 30- and 90-d post-transplant, as well as initial function, endoscopic appearance, rejection episodes, or transplant pancreatitis between HTK and UW as preservation solutions in small bowel and multivisceral grafts (24). However, HTK is cheaper and has been proposed by the authors to improve the flushing of the microvasculature due to its low viscosity as observed through surgical loupes by explant surgeons. Back table procedure. Isolated small bowel grafts require little revision at the back table. The back table vascular reconstruction of the composite small bowel–pancreas graft has been shown in Fig. 2. For the composite liver–small bowel grafts, the back table procedure includes the preparation of vena cava, the over-sewing of the duodenal stump, removal of the spleen, and revision and suturing of the Carrel patch to a previously prepared segment of thoracic aorta (Fig. 4; 25). For multivisceral grafts, the stump of the transected gastroesophageal junction is oversewn and a pyloroplasty is performed at the back table. However, the vascular conduits to lengthen the graft arterial supply or the venous drainage are preferably first anastomosed to the recipient infrarenal aorta and portal vein or IVC rather than the graft vessels at the back table for

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A

B

D

C

the technical convenience. With modified “liversparing” multivisceral grafts, the liver is separated at the back table.

Recipient techniques Recipient preparation

A targeted evaluation of the recipients begins with thorough medical and surgical history and physical examination, comprehensive assessment of patient nutritional status, biochemical profile, and hypercoagulability studies. GI anatomic and functional assessment includes radiologic, endoscopic, and histologic examinations. GI motility studies are required for recipients with pseudo-obstruction syndromes to define the extent of the disease. It is mandatory to perform visceral angiography to assess the extent of splanchnic thrombosis as well as to guide the type of the visceral transplant needed. Radiologic mapping of the central veins of major upper and lower trunk is essential for the establishment of the venous access at the time of transplantation. Liver biopsy is required for the decision-making for the replacement of the liver. The extent of assessment of cardiopulmonary and other body systems is dictated by patient age, past medical history, and underlying pathologies (18). Recipient techniques

The abdominal incision for the recipient includes a midline laparotomy with unilateral or bilateral extensions. The recipient procedure is usually

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Fig. 4. Arterial reconstruction in the liver–small bowel transplantation. Figures depicting an infrarenal aortic graft using donor thoracic aorta in a pediatric liver–small bowel transplantation. Clockwise: (A) and (B) tailoring the Carrel patch during back table procedure; (C) tailoring jump graft at the recipient side; and (D) anastomosis of the jump graft between the already tailored donor’s and the recipient’s sides. Photographs were taken with permission from the Thomas E. Starzl Transplantation Institute, Children’s Hospital of Pittsburgh, PA, USA.

complicated with the presence of extensive abdominal adhesions and loss of abdominal domain due to often multiple previous operations such as resections, lengthening operations, and treatment of complications as well as underlying diseases such as portal hypertension, venous thrombosis or desmoid tumors. Care should be taken to avoid donor–recipient size mismatch. The individual operative techniques in recipients of each main ITx-prototype are described as following. Isolated small bowel transplantation. The surgical procedure usually includes the native enterectomy in cases of functional disease or neoplasm, to identify the proximal and distal functioning remnants of the small bowel. The arterial reconstruction is performed through the anastomosis of the donor SMA, inclusive a small aortic patch, to the infrarenal aorta. For the venous reconstruction, the donor SMV is drained into the recipient portal vein, recipient SMV or splenic vein, or the recipient IVC (Fig. 5). The venous drainage into the portal system should always be preferred due to its physiologic and possible immunologic advantages but depends on the technical feasibility of accessing the recipient portomesenteric axis (23). The caval venous drainage should be limited to recipients with frozen hepatic hilus, portal vein thrombosis, significant hepatic fibrosis, and prior intestinal transplants. In patients with modest portal hypertension presented with mild splenic enlargement, for whom the decision has been made to perform isolated small

Operative techniques of intestinal transplantation

Fig. 5. Vascular reconstruction in the isolated small bowel transplantation. From left to right: an isolated small bowel graft, venous drainage into the inferior vena cava, venous drainage into portal system.

bowel transplantation in the absence of low platelet counts, gastroesophageal varices, and intrahepatic cholestasis, the venous outflow should be drained into the recipient IVC (26). The intestinal continuity is restored through proximal and distal anastomoses, usually as an end-to-end jejunojejunostomy and end-to-side ileocolostomy, with the construction of a temporary vent “chimney” – Schornstein – ileostomy (Bishop–Koop ileostomy) to access the ileum for the purpose of zoom endoscopic surveillance and diagnostic biopsy. A tube jejunostomy may be placed in the proximal allograft jejunum for the purpose of decompression and, later on, the initiation of enteral feeding. The ileostomy can be taken down after the adequate restoration of oral nutrition, the stabilization of the immunosuppression therapy, and in the absence of the need for frequent endoscopic surveillance. Other less frequently used methods that include the construction of a “Thiry-Vella-loop” (an excluded jejunal loop from the graft which is then exteriorized at both ends to gain access for biopsies from the graft; 27), (modified) “Paul-Mikulicz ileostomy” (a proximal side-to-side ileo-ileal anastomosis with doublebarrel ileostomy to gain access to both the donor’s and the recipient’s ileum; 28), and the “Blind Innsbruck Ostomy” (a side-to-end ileocolostomy 20 cm from the end of the graft, with the distal part of the graft brought out as a stoma for the purpose of graft monitoring, which is later excluded from GI continuity; 29) have also been described. Lymphatic leak, which is due to the interruption of lymphatic channels at the time of organ

procurement, may occur early after transplantation and initiation of enteral feeding and is usually self-limited under low or fat-free diet and use of medium-chain triglyceride enteral formula (30). The self-limited nature of the process reflects the spontaneous reconstitution of lymphatic collaterals that connect the donor and recipient lymphatic system. The anastomosis of the major donor and recipient lymphatic channel has been described in the experimental setting (31). Liver–small bowel transplantation. The arterial reconstruction of the composite liver–small bowel graft is performed through an arterial “Carrel” patch fashioned around the orifices of the CT and SMA, which is anastomosed to the recipient infrarenal aorta. The Carrel patch can be lengthened via an aortic or iliac interposition (Figs. 4 and 6). The caval drainage of the donor liver is reconstructed using the piggyback technique. As the native stomach, pancreaticoduodenal axis, and spleen are preserved in this technique, a venous drainage for these native organs has to be fashioned, either into the graft’s portal vein or in the form of a portocaval shunt (7). The GI continuity is performed as with the isolated small bowel transplantation. Multivisceral transplantation. Exenteration of the entire native GI tract makes space for the multivisceral transplantation. In the full multivisceral transplant, the arterial inflow and caval venous outflow are reconstructed as with the composite liver–small bowel transplantation. Likewise, there

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A report of 500 consecutive small bowel and multivisceral transplants at the University of Pittsburgh (20) shows a significant trend towards some of the above-mentioned modifications of donor and recipient surgical techniques in each main prototype during three recent eras beginning from 1990 through 2009, including the significant increase in portal venous drainage in the isolated small bowel transplantation, the inclusion of donor duodenum with full pancreas as well as the use of the reducedsize grafts in liver–small bowel transplantation, and significantly more modified multivisceral grafts.

Fig. 6. Infrarenal aortic graft. Three-dimensional angiogram of a patient who received a composite liver–small bowel allograft with an infrarenal aortic graft. Courtesy of Dr. AbuElmagd.

is no portal vein anastomosis needed, as the donor portal axis remains intact during the allograft procurement. The GI continuity is re-established through the anastomosis of the graft stomach to the recipient gastric cuff or abdominal esophagus proximally; the distal reconstruction is similar to that for isolated small bowel transplantation. In patients with a normal native liver, a modified “liver-sparing” multivisceral procedure is performed, excluding the donor liver as part of the multivisceral allograft (Fig. 1, inset). In this technique, the native liver, spleen, pancreas, and a C loop of duodenum are retained. The graft portal outflow has to be drained into the recipient portal circulation. Biliary drainage from the native liver as well as from both pancreases is accomplished with a side-to-side donor-to-recipient duodenal anastomosis (32). Concomitant preservation of pancreaticoduodenal complex eliminates the risk of biliary complications and helps in better glucose homeostasis. Through the preservation of native spleen and the portosplenic circulation, this modification has been shown to be associated with increased survival, reduced risk of the post-transplant lymphoproliferative disease (PTLD), life-threatening infections, and graft-vs.-host disease (GVHD) with no significant impact on graft loss due to rejection (33). In cases of native pancreaticoduodenectomy, the biliary drainage is reconstructed through performing a duct-to-duct anastomosis.

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Abdominal wall management. Loss of the abdominal domain in ITx recipients due to extensive adhesions secondary to multiple prior operations, abdominal wall scarring due to ostomies, laparotomies, fistulas, and desmoids, shortage of appropriate recipient-size-matched donors, and post-perfusion graft edema make the primary closure of the abdominal wall after ITx challenging. A primary tension-free fascial closure is achievable in approximately 50–85% of recipients. Aside from reduced-sized grafts to facilitate the primary closure of the abdomen, which are used mainly for pediatric donors, different strategies have been employed to reconstruct the abdominal wall and enlarge the abdominal domain. These include the use of pre-transplant abdominal tissue expanders, temporary coverage, and staged abdominal closure using absorbable and nonabsorbable mesh, bioengineered skin equivalents, acellular dermal matrix, rectus muscle fascia, splitthickness, or full-thickness skin grafts and finally simultaneous abdominal wall transplantation as a vascularized composite graft (34, 35). Abdominal wall transplantation allows primary skin closure and hence early mobilization and rehabilitation of the recipient; the drawbacks include the need for complex vascular reconstruction, significantly longer operative and anesthesia time as well as high morbidity. For the purpose of abdominal wall transplantation, an abdominal flap is lifted up together with the underlying bilateral rectus abdominis muscles and a small part of the oblique muscles and the deep muscular sheet, together with the thin parietal layer of peritoneum. The graft can be removed en bloc with the femoral and iliac vessels, with a short segment of distal aorta and IVC (36). Alternatively, the deep inferior epigastric vessels may be prepared and transected at their origin form the iliac vessels at the end of the organ recovery (37). Cold pre-fusion and conservation are carried out as with other organs. The abdominal wall transplantation starts at the end of the ITx: The vessels of the abdominal wall graft can be

Operative techniques of intestinal transplantation implanted like a kidney allograft into the recipient’s common iliac artery and vein. Alternatively, the donor epigastric pedicles can be anastomosed end-to-end with the recipient epigastric vessels using a microsurgical technique with the help of microscope. The surgical procedure will be then completed with the ileostomy formation, suturing of the deep and superficial muscular fascia and cutaneous suturing. The function of the abdominal wall graft is monitored by biopsies of the skin of the flap within the first two wk and subsequently only by examination of the color of the skin (38). The use of avascular rectus muscle allofascia is reported to provide the native strength and structure of a muscle, not immunogenic, and also costeffective (34). The following section deals with a rapid survey of some technical challenges and topics of debate in the field of ITx. Inclusion of colon and ileocecal valve

Patients without the ileocecal valve, especially pediatric recipients, have principally frequent lessformed stools and are therefore prone to dehydration. The addition of the ileocecal valve and right hemicolon would provide more physiologic GI situation, thus providing a better quality of life in recipients. Although initial reports had considered the inclusion of colon as a potential risk factor for morbidity and mortality (39), it was later shown not to affect the clinical outcome (40, 41). A more recent single-center retrospective cohort of 245 consecutive primary ITx recipients, among whom 93 received a donor colon, showed that this procedure carries no obvious additional morbidity or mortality risk, particularly with respect to graft survival. A subset analysis of the recipients of multivisceral transplants suggested a more favorable impact of including the donor colon on graft survival; children receiving donor colons had a significantly higher percentage of formed stools after stoma closure. The authors recommended that the inclusion of donor colonic segment be actively considered for ITx recipients (42). A sphincter-preserving pull-through technique with en bloc colon and ITx has been reported with the potential to improve allograft absorptive function and quality of life in patients with resected or strictured colorectum and preserved anal sphincter (43). Transplantation of the spleen

If the native spleen is removed along with other viscera during the recipient operation in multivisceral

transplant, the recipient will be left asplenic. Asplenia makes the patients prone to an increased risk of sepsis with encapsulated bacteria. On the other hand, animal studies have shown the donor splenic transplantation to induce donor-specific tolerance (44, 45). With the rationale of protection from the risk of sepsis associated with the asplenic state, especially in pediatric recipients, as well as testing its tolerogenic effects in pediatric and adult recipients, one center has started to routinely add the spleen to the multivisceral grafts since 2001. Although no significant differences in rate of infectious complications were observed between the multivisceral recipients who received a donor spleen vs. who did not, a univariate analysis yielded superiority in “freedom from any rejection” and “freedom from moderate or severe rejection” for the spleen recipients without significantly increasing the risk of GVHD. The authors concluded that the allogenic spleen seems to show some protective effects on small bowel rejection, leaving the debate over the precise role of the allogenic spleen open for further investigation (46). Living donor ITx

In the largest published case-series on the issue, 13 living donor small bowel grafts were transplanted in 10 pediatric recipients, including five cases of combined living donor intestinal and liver transplants (CLDILTx), two of whom were recipients of simultaneous non-composite liver–small bowel transplants. Small bowel grafts consisted of an ileum segment 150 cm in length, whereas liver grafts were standard left lateral liver lobes. The donors were selected from the best human leukocyte antigen (HLA) match and included 10 mothers, one father, one maternal uncle, and one maternal grandmother. In CLDILTx recipients, the patient survival at one and two yr was 100%, the liver graft survival 100%, and the bowel graft survival 80%; the patient who lost the initial intestinal graft was successfully retransplanted from another living-related donor. In living donor isolated intestinal transplantation (LDITx) recipients, the patient and graft survival rates at one and three yr were 60% and 50%, respectively. None of donors reported changes in life style, work habits, or psychologic condition after donation. The authors concluded that CLDILTx can be performed successfully simultaneously or sequentially to reduce the morbidity and mortality on the waiting list, especially in children with intestinal failure who develop acutely decompensated chronic liver failure. These patients can be effectively treated initially with segmental liver transplants to

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stabilize their condition, followed by an elective ITx from the same living-related donor few weeks later. LDITx have been suggested to be considered to rescue the pediatric patients with lack of central venous access as an alternative to cadaveric ITx. However, the results were disappointing in the setting of children ≤6 kg with high rate of acute irreversible rejection; the authors have therefore recommended a minimum weight >8 kg (47). Retransplantation

Although Re-ITx has been associated with a significantly higher morbidity and mortality, acceptable outcomes can be achievable with more recent changes in immunosuppression protocols, technical modifications, improved monitoring of infectious diseases, and desensitization protocols in sensitized cases, in carefully selected patients. In the report of 500 intestinal and multivisceral transplantations from the University of Pittsburgh (20), there has been a total of 47 (10%) retransplants, with the rejection being the leading indication. With higher early post-transplant attrition rate, the five-yr survival was similar to the primary allografts; retransplantation of liver-contained visceral allografts achieved better five-yr survivals compared with the liver-free visceral grafts. When the retransplantation is indicated, enterectomy and withdrawal of immunosuppression followed by a period of home parenteral nutrition should be preferably attempted well ahead of retransplantation (48). For the purpose of graft enterectomy, the use of preoperative interventional embolization to decrease blood loss and demarcating the graft from the native bowel at the time of graft enterectomy has been reported to be useful (49). Conclusion

The evolution of ITx from a highly experimental method with unsatisfactory results into an established therapeutic modality with acceptable patient and graft survival rates during the last two decades has been achieved through standardization in surgical techniques, improvements in immunosuppressive and induction protocols, and postoperative patient care. From a surgical technical point of view, all different types of small bowel containing transplants are categorized into three main prototypes, that is, isolated small bowel, liver–small bowel, and multivisceral transplantation, with their own indications. Aside from technical modifications, and donor and recipient procedures, abdominal wall management, inclusion of colon and ileocecal

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valve, transplantation of the spleen, living donor transplantations, and retransplantation have been among the more recent surgical technical topics of discussion in the literature. Future studies to acquire more evidence-based facts regarding the above-mentioned topics may further define their role in the field of ITx. References 1. CARREL A. Landmark article, Nov 14, 1908: Results of the transplantation of blood vessels, organs and limbs. JAMA 1983: 250: 944. 2. LILLEHEI RC, GOOTT B, MILLER FA. The physiological response of the small bowel of the dog to ischemia including prolonged in vitro preservation of the bowel with successful replacement and survival. Ann Surg 1959: 150: 543. 3. STARZL TE, KAUPP HA Jr. Mass homotransplantations of abdominal organs in dogs. Surg Forum 1960: 11: 28. 4. STARZL TE, ROWE MI, TODO S et al. Transplantation of multiple abdominal viscera. JAMA 1989: 261: 1449. 5. DELTZ E, SCHROEDER P, GEBHARDT H, GUNDLACH M, ENGEMANN R, TIMMERMANN W. First successful clinical small intestine transplantation. Tactics and surgical technic. Chirurg 1989: 60: 235.  Y, JAN D et al. Small-bowel trans6. GOULET O, REVILLON plantation in children. Transplant Proc 1990: 22: 2499. 7. GRANT D, WALL W, MIMEAULT R et al. Successful smallbowel/liver transplantation. Lancet 1990: 335: 181. 8. ABU-ELMAGD K. The history of intestinal transplantation. In: NAKIM NS, PAPALOIS VE eds. The History of Organ and Cell Transplantation. London: Imperial College Press, 2003: 171. 9. ABU-ELMAGD K, BOND G, REYES J, FUNG J. Intestinal transplantation: a coming of age. Adv Surg 2002: 36: 65. 10. ABU-ELMAGD KM. The small bowel contained allografts: existing and proposed nomenclature. Am J Transplant 2011: 11: 184. 11. GRANT D, ABU-ELMAGD K, REYES J et al. Intestine Transplant Registry. 2003 report of the intestine transplant registry: a new era has dawned. Ann Surg 2005: 241: 607. 12. VIANNA RM, MANGUS RS. Present prospects and future perspectives of intestinal and multivisceral transplantation. Curr Opin Clin Nutr Metab Care 2009: 12: 281. 13. BUENO J, ABU-ELMAGD K, MAZARIEGOS G, MADARIAGA J, FUNG J, REYES J. Composite liver-small bowel allografts with preservation of donor duodenum and hepatic biliary system in children. J Pediatr Surg 2000: 35: 291. 14. SUDAN DL, IYER KR, DEROOVER A et al. A new technique for combined liver/small intestinal transplantation. Transplantation 2001: 72: 1846. 15. DE VILLE DE GOYET J, MITCHELL A, MAYER AD et al. En bloc combined reduced-liver and small bowel transplants: from large donors to small children. Transplantation 2000: 69: 555. 16. REYES J, FISHBEIN T, BUENO J, MAZARIEGOS G, ABUELMAGD K. Reduced-size orthotopic composite liver-intestinal allograft. Transplantation 1998: 66: 489. 17. ABU-ELMAGD KM. Intestinal transplantation for short bowel syndrome and gastrointestinal failure: current consensus, rewarding outcomes, and practical guidelines. Gastroenterology 2006: 130: S132. 18. ABU-ELMAGD K. Intestinal transplantation: indications and patient selection. In: LANGNAS AN, GOULET O, QUIGLEY EMM, TAPPENDEN KA eds. Intestinal Failure:

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20.

21.

22.

23.

24.

25.

26.

27.

28.

29.

30.

31.

32.

33.

Diagnosis, Management and Transplantation. Malden, MA: Blackwell Publishing, 2008: 245. WUNDERLICH H, BROCKMANN JG, VOIGT R et al. Commission of Organ Donation and Removal German Transplantation Society. DTG procurement guidelines in heart beating donors. Transpl Int 2011: 24: 733. 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: 567. ABU-ELMAGD K, FUNG J, BUENO J et al. Logistics and technique for procurement of intestinal, pancreatic, and hepatic grafts from the same donor. Ann Surg 2000: 232: 680. ROGIERS X, MALAGO M, GAWAD K et al. In situ splitting of cadaveric livers. The ultimate expansion of a limited donor pool. Ann Surg 1996: 224: 331. TZAKIS AG, TODO S, REYES J, NOUR B, FUNG JJ, STARZL TE. Piggyback orthotopic intestinal transplantation. Surg Gynecol Obstet 1993: 176: 297. MANGUS RS, TECTOR AJ, FRIDELL JA, KAZIMI M, HOLLINGER E, VIANNA RM. Comparison of histidine-tryptophanketoglutarate solution and University of Wisconsin solution in intestinal and multivisceral transplantation. Transplantation 2008: 86: 298. REYES J, SELBY R, ABU-ELMAGD K et al. Intestinal and multiple organ transplantation. In: AYRES SM, HOLBROOK PR, SHOEMAKER WC eds. Textbook of Critical Care. Philadelphia, PA: W.B. Saunders Company, 1995: 1986. MAZARIEGOS G, BOND G, ABU-ELMAGD K, REYES J, COSTA G. Intestinal failure and visceral transplantation: a new era of colossal achievement. In: MATARESE LE, STEIGER E, SEIDNER DL eds. Intestinal Failure and Rehabilitation: A Clinical Guide. Boca Raton, FL: CRC Press, 2005: 295. LEVARD G, REVILLON Y, ARHAN P et al. Motility of the transplanted small bowel: a manometric study in the piglet. Eur J Pediatr Surg 1994: 4: 98. TSAI MS, LIN WH, HSU WM et al. Modified Paul-Mikulicz ileostomy in a Swine model of isolated small bowel transplantation. J Surg Res 2010: 164: 329. KONIGSRAINER A, LADURNER R, IANNETTI C et al. The ‘Blind Innsbruck Ostomy’, a cutaneous enterostomy for long-term histologic surveillance after small bowel transplantation. Transpl Int 2007: 20: 867. ABU-ELMAGD K, REYES J, FUNG J. Transplantation of the human intestine: the forbidden organ. Curr Opin Organ Transplant 1998: 3: 286. KELLERMANN R, ZHONG R, KIYOCHI H et al. Lymphatic reconstruction has a long-term benefit after intestinal transplantation in rats. Transplantation 1998: 66: S25. ABU-ELMAGD K, REYES J, BOND G et al. Clinical intestinal transplantation: a decade of experience at a single center. Ann Surg 2001: 234: 404. CRUZ RJ Jr, COSTA G, BOND G et al. Modified “liver-sparing” multivisceral transplant with preserved native spleen,

34.

35.

36. 37.

38.

39.

40.

41.

42.

43.

44.

45.

46.

47.

48.

49.

pancreas, and duodenum: technique and long-term outcome. J Gastrointest Surg 2010: 14: 1709. GERLACH UA, PASCHER A. Technical advances for abdominal wall closure after intestinal and multivisceral transplantation. Curr Opin Organ Transplant 2012: 17: 258. SHETH J, SHARIF K, LLOYD C et al. Staged abdominal closure after small bowel or multivisceral transplantation. Pediatr Transplant 2012: 16: 36. LEVI DM, TZAKIS AG, KATO T et al. Transplantation of the abdominal wall. Lancet 2003: 361: 2173. CIPRIANI R, CONTEDINI F, SANTOLI M et al. Abdominal wall transplantation with microsurgical technique. Am J Transplant 2007: 7: 1304. BEJARANO PA, LEVI D, NASSIRI M et al. The Pathology of full-thickness cadaver skin transplant for large abdominal defects: a proposed grading system for skin allograft acute rejection. Am J Surg Pathol 2004: 28: 670. TODO S, REYES J, FURUKAWA H et al. Outcome analysis of 71 clinical intestinal transplantations. Ann Surg 1995: 222: 270. GOULET O, AUBER F, FOURCADE L et al. Intestinal transplantation including the colon in children. Transplant Proc 2002: 34: 1885. LACAILLE F, VASS N, SAUVAT F et al. Long-term outcome, growth and digestive function in children 2 to 18 years after intestinal transplantation. Gut 2008: 57: 455. KATO T, SELVAGGI G, GAYNOR JJ et al. Inclusion of donor colon and ileocecal valve in intestinal transplantation. Transplantation 2008: 86: 293. EID KR, COSTA G, BOND GJ et al. An innovative sphincter preserving pull-through technique with en bloc colon and small bowel transplantation. Am J Transplant 2010: 10: 1940. SUZUKI H, LI XH, MIYAMOTO M, SANO T, HATTORI Y, YAMASHITA A. Induction of transplantation tolerance in adult rats by vascularized spleen transplantation. Transplantation 1997: 64: 650. DUNCAN WR, BITTER-SUERMANN H, STEPKOWSKI SM. Induction of transplantation tolerance in rats by spleen allografts. III. The role of T suppressor cells in the induction of specific unresponsiveness. Transplantation 1987: 44: 553. KATO T, TZAKIS AG, SELVAGGI G et al. Transplantation of the spleen: effect of splenic allograft in human multivisceral transplantation. Ann Surg 2007: 246: 436. GANGEMI A, TZVETANOV IG, BEATTY E et al. Lessons learned in pediatric small bowel and liver transplantation from living-related donors. Transplantation 2009: 87: 1027. MAZARIEGOS GV, SOLTYS K, BOND G et al. Pediatric intestinal retransplantation: techniques, management, and outcomes. Transplantation 2008: 86: 1777. FAN J, TEKIN A, NISHIDA S et al. Preoperative embolization of the graft superior mesenteric artery assists graft enterectomy in intestinal transplant recipients. Transplantation 2012: 94: 89.

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