Background: Short bowel syndrome (SBS) is a state of malabsorption resulting from massive small bowel resection leading to parenteral nutrition (PN) dependency. Considerable advances have been achieved in the medical and surgical management of SBS over the last few decades. Methods: This review discusses in detail the surgical approach to SBS. Results: Widespread use of PN enables long-term survival in patients with intestinal failure but at the cost of PN-associated life-threatening complications including catheter-associated blood stream infection, venous thrombosis, and liver disease. The goal of management of intestinal failure due to SBS is to enable enteral autonomy and wean PN by means of a multi-disciplinary approach. Availability of modified enteral feeding formulas have simplified nutrition supplementation in SBS patients. Similarly, advances in the medical field have made medications like growth hormone and glucagon-like peptide (GLP2) available to improve water and nutrient absorption as well as to enable achieving enteral autonomy. Autologous gastrointestinal reconstruction (AGIR) includes various techniques which manipulate the bowel surgically to facilitate the bowel adaptation process and restoration of enteral nutrition. Ultimately, intestinal transplantation can serve as the last option for the cure of intestinal failure when selectively applied. Conclusion: SBS continues to be a challenging medical problem. Best patient outcomes can be achieved through an individualized plan, using various AGIR techniques to complement each other, and intestinal transplantation as a last resort for cure. Maximum benefit and improved outcomes can be achieved by caring for SBS patients at highly specialized intestinal rehabilitation centers.

Kurzdarmsyndrom

KDS

Parenterale Ernährung

PE

Autologe gastrointestinale Rekonstruktion

AGIR

Longitudinale intestinale Verlängerungsoperation

LILT

Serielle transverse Enteroplastie

STEP

Ultrakurzdarmsyndrom

USBS

Hintergrund: Das Kurzdarmsyndrom (KDS) stellt einen Zustand der Malabsorption dar, der aus einer massiven Dünndarmresektion, die zur Abhängigkeit von parenteraler Ernährung (PE) führt, resultiert. In den letzten Jahrzehnten wurden erhebliche Fortschritte in der internistischen und chirurgischen Behandlung des KDS erreicht. Methoden: Diese Übersicht beschreibt im Detail die chirurgische Herangehensweise an das KDS. Ergebnisse: Die weit verbreitete Verwendung von PE ermöglicht ein Langzeitüberleben bei Patienten mit Darmversagen, jedoch auf Kosten der PE-assoziierten lebensbedrohlichen Komplikationen wie Katheter-assoziierter Blutvergiftung, Venenthrombose und Lebererkrankung. Das Ziel des Managements von Darmversagen aufgrund von KDS ist die Ermöglichung einer enteralen Autonomie und die Entwöhnung von der PE durch einen multi-disziplinären Ansatz. Die Verfügbarkeit von modifizierten enteralen Ernährungsformen hat die ergänzende Nährstoffversorgung von KDS-Patienten vereinfacht. Gleichzeitig haben Fortschritte in der Medizin dafür gesorgt, dass das Wachstumshormon und Glucagon-like-Peptide (GLP2) zur medikamentösen Behandlung zur Verfügung stehen, um die Wasser- und Nährstoffabsorption zu verbessern und das Erreichen einer enteralen Autonomie zu ermöglichen. Die autologe gastrointestinale Rekonstruktion (AGIR) umfasst verschiedene Techniken, die den Darm chirurgisch manipulieren, um den Anpassungsprozess des Darms und die Wiederherstellung der enteralen Ernährung zu erleichtern. Letztlich kann eine Darmtransplantation als letzte Option zur Heilung von Darmversagen dienen, wenn diese selektiv angewendet wird. Schlussfolgerung: Das KDS stellt weiterhin eine schwierige medizinische Herausforderung dar. Die besten Ergebnisse für die Patienten können mittels einer individuellen Planung, in deren Rahmen sich verschiedene AGIR-Techniken ergänzen, sowie der Darmtransplantation als letzte Möglichkeit der Heilung erreicht werden. Maximaler Nutzen und verbesserte Ergebnisse können durch die Betreuung von Patienten mit KDS in hochspezialisierten Darmzentren erreicht werden.

Since its introduction in the late 1960's, parenteral nutrition (PN) has been the mainstay of therapy for patients with intestinal failure [1]. Advances in recent years have improved survival in PN-dependent patients, primarily through a multi-disciplinary approach including various medical and surgical rehabilitation strategies aimed at achieving enteral autonomy [2, 3, 4]. Yet, 19-26% of patients continue to be permanently PN-dependent and develop a high rate of complications that lead to high mortality rates of 13-38% by 2-5 years following the development of intestinal failure [5, 6].

This review aims at discussing the various strategies involved in the surgical approach to short bowel syndrome (SBS).

Initial surgical management of patients at risk for SBS includes every attempt to conserve as much bowel as possible even though planned serial ‘second look' surgeries may be required to evaluate for viability of marginal bowel segments. Following recovery from the initial episode and return of bowel function, administration of enteral feeds and, if possible, early stoma closure are recommended to enhance adaptation and help in weaning PN [7]. In almost 75% of patients with SBS, intestinal adaptation precludes the need for surgical rehabilitation and is often sufficient to support growth and long-term survival [8]. However, since adaptation is a slow process extending over 6 months to 2 years, patients should be given adequate time to reach their full adaptive potential prior to any surgical consideration [8, 9].

Bowel adaptation is a remodeling process, involving compensatory mechanisms aimed at improving the absorptive capacity of the remnant bowel following intestinal loss. Increase in the intestinal mass and surface area occurs through enterocyte and crypt cell proliferation, increase in microvilli with taller villi and deeper crypts, and hyperplasia and hypertrophy of the smooth muscle layers. Adaptation is an ongoing process that begins 24-48 h after surgical resection, progressing rapidly during the initial 4-24 months following intestinal loss, and can take years to complete [10, 11]. Following intestinal resection the motor activity of the bowel is also disrupted for a few months [12]. Studies have demonstrated a shorter duration of migrating motor complex cycle and fed pattern after resection [13]. Once this initial phase is over, motor adaptation begins, more prominently in the jejunum than in the ileum. Combination of the structural and motor adaptation results in prolonged intestinal transit time and improved absorption by individual enterocytes.

Various factors influencing intestinal adaptation include gastrointestinal regulatory peptides, growth factors, hormones, and cytokines in addition to tissue factors including immunity, blood flow, and neural influences [14, 15]. The extent of resection also strongly influences the degree of intestinal adaptation and thereby the ability to wean PN [16]. Although the ileum has a greater adaptive capacity than the jejunum, massive ileal resection has a significantly worse impact than jejunal resection, as the ileum plays an important role in electrolyte and water absorption as well as absorption of vitamin B12, bile salts, and fatty acids [17, 18]. Younger patients (infants and neonates) are much more likely to adapt due to periods of rapid bowel growth as evidenced by nearly a doubling of the bowel length in the first 18 months of life, and hence they are more likely to wean off PN [19, 20].

In some patients, however, rapid bowel growth results in excessive dilatation of the remnant bowel resulting in dysmotility and stasis which promotes bacterial overgrowth contributing to malabsorption, bacterial translocation with systemic infection, and ultimately liver injury [21, 22]. This may further negatively impact ongoing adaptation and thus the ability to wean PN [23, 24]. Since bowel dilatation is a natural sequel of adaptation, surgery should be deferred unless dilatation causes recurrent episodes of bacteremia [25, 26]. It is noted that bowel dilatation occurs more commonly in younger patients who more often are candidates for surgical rehabilitation as compared to adults [27].

Most centers are conservative in recommending intestinal-lengthening procedures, only offering it as an adjunct to nutritional and medical management in patients who have reached a plateau in weaning PN. When allowing spontaneous intestinal adaptation, frequent assessment is needed to reassure adequate growth while avoiding intestinal failure-associated liver disease (IFALD) and other serious complications of PN such as recurrent line infections and loss of venous access [28, 29].

Due to the PN-associated comorbidities, the initial goal in management of patients with intestinal failure is to enable PN weaning. Autologous gastrointestinal reconstruction (AGIR) further facilitates the adaptation process and attempts to reverse complications of PN. AGIR can be considered once maximal adaptation is achieved and further weaning of PN fails or with recurrence of malabsorption in previously achieved partial or complete adaptation as demonstrated by stable fluid and/or calorie requirements from intravenous supplementation [30, 31]. With the onset of PN-induced advanced liver disease manifested by coagulopathy and portal hypertension, intestinal transplantation remains the only salvageable option [32, 33].

The principle of AGIR relies on bowel dilatation resulting from post-resectional adaptation [34] and the ability to manipulate this dilated bowel surgically to improve the dysmotility and the absorption, thereby facilitating enteral autonomy [35]. Of the various methods of reconstruction, tapering enteroplasty, Bianchi's longitudinal intestinal lengthening and tailoring (LILT), and the serial transverse enteroplasty (STEP) have gained wide acceptance [34]. The main predictor of the ability to achieve enteral autonomy following AGIR is the final length of the remaining small intestine [36, 37]. It is now well accepted that with a remnant bowel length < 40 cm, the probability of permanent PN dependency is fairly high [38]. In such cases, where the chance of spontaneous adaptation is minimal, creating controlled obstruction to actively generate bowel dilatation is suggested in order to be able to perform AGIR surgery later [39].

Careful patient selection is essential to avoid unnecessary operations, since some infants especially with low birth weight and necrotizing enterocolitis as the etiology leading to a very short bowel remnant may wean off PN without any AGIR procedures at all [38].

In a select group of patients, despite long remnants of small bowel, rapid transit results in increased ileostomy output due to absence of ileocecal valve (ICV) and colon. Placing a reverse intestinal segment proximal to the ileostomy in such cases can suffice to slow the transit and facilitate nutrient and fluid absorption. These patients often wax and wane clinically, requiring nutrient and fluid replacements periodically [40]. This concept of reversed intestinal segment dates back to the 1880's [41]; however, it received more popularity in the latter half of the 20th century as one of the earliest surgical procedures designed to slow intestinal transit [42, 43].

An antiperistaltic bowel loop, by its virtue, creates partial mechanical obstruction and delays myoelectric activity in the distal segment, thus slowing the transit to enhance nutrient absorption [44].

Although smaller case series have suggested a length of the reversed segment between 10-15 cm for adults and around 3 cm for children for maximal benefit [45, 46], uncertainty in establishing the ideal length and location of the reversed intestinal segment produced variable results when applied clinically. Despite the purported benefits, this technique failed to gain popularity due to the potential risk of obstruction with longer reversed segments [47]. Obviously, this technique cannot be used when the remnant bowel length is <25 cm.

A recent largest series of SBS patients treated with reversed segment concluded that a distally placed reversed intestinal segment of 10-12 cm is an appealing and safe conservative alternative to small bowel transplantation in adults with ‘permanent' PN dependency, with a minimum small bowel length (SBL) of 25 cm, and without chronic liver failure [48]. Unlike other procedures, it can be performed regardless of the bowel diameter with the expectation of almost half of the patients to be weaned from PN.

When remnant bowel represents 10% (with ICV) or 20% (without ICV) of predicted SBL, it is termed ultra-short bowel syndrome (USBS). It usually arises from massive small bowel resection, congenital jejuno-ileal atresia, or in rare cases of vanishing gastroschisis. In such cases AGIR should be considered as a complementary rather than a rescue procedure [49].

A recent small case series of patients with USBS due to jejunal atresia has shown that persistent proximal obstruction with sham feeds and periodic gastrostomy tube clamping helps to dilate the proximal jejunal remnant and optimizes the potential for AGIR [50]. Following lengthening procedure (STEP), the SBL increases by an average of nearly 300% in comparison to the average expected increase of 37% without therapy. Sham feeds and gastrostomy clamping alone produced a mean SBL increase of 159%, suggesting that the technique can dramatically augment gut growth within the first few months of life compared to the rate of expected normal growth.

Different AGIR options (table 1) must be tailored individually according to the length and type of residual intestine, but in certain situations combination of various techniques may prove more beneficial than a single procedure. USBS is a perfect example of this situation. Enteral autonomy has been reported in a patient with a remnant of 5 cm of the jejunum and entire colon with definitive surgery aimed at lengthening the remnant jejunum and part of the colon (Bianchi technique), delaying transit with antiperistaltic anastomosis of the lengthened colon, and increasing the rectal capacity by creating a hypotonic reservoir proximal to the rectum with a sigmoid J pouch in order to diminish both urgency and frequency of stools [51]. This report indicated that similar to the small bowel, colonic duplication is also technically feasible. A beneficial delay in intestinal transit can be achieved with careful antiperistaltic colonic interposition, despite prior reports of unpredictability and fatal obstruction [52].

Table 1

Different operative approaches for SBS including advantages and limitations of the different techniques

Different operative approaches for SBS including advantages and limitations of the different techniques
Different operative approaches for SBS including advantages and limitations of the different techniques

In the event of a too short remnant small bowel precluding AGIR, isoperistaltic colon interposition can be a useful technique in patients with USBS [53]. Under exceptional circumstances the colon adopts an important metabolic role, with bacterial metabolism and fermentation within the colon exerting a significant trophic effect on the mucosa of the small intestine and colon [54]. The colonic segment adapts to its new location with hypertrophy and hyperplasia of the mucosal crypt glands and developing contractile responses similar to those of the remaining small bowel [55, 56]. However, complications arising from colonic dilatation and enterocolitis within the transposed segment make this procedure rather unappealing.

One of the simpler procedures of AGIR is a tapering enteroplasty, which involves excising a wedge of the antimesenteric border of the dilated bowel followed by suturing the remnant bowel into a tube [57]. This reduces the diameter of the dilated bowel and facilitates an early return of effective peristalsis. This procedure was preferred to resection for managing dilated bowel in jejunal atresia [58]. Since tapering enteroplasty optimizes bowel caliber at the expense of loss of significant mucosal absorptive surface, it should be reserved to tackle stasis and malabsorption in a dilated bowel only in the presence of adequate intestinal length. It can also be a procedure of choice when vascular anatomy of the dilated bowel does not permit bowel division for a lengthening procedure. Tapering results in a long suture line that may increase the risk of anastomotic leakage.

The technique of intestinal plication was designed by circumferential plication of the dilated bowel after folding the redundant antimesenteric wall into the lumen to avoid the long anastomotic suture line of enteroplasty and also preserve the mucosal mass which is an important consideration in SBS [59]. With long-term follow-up, development of obstruction and redilatation due to unraveling from suture breakdown has been reported.

One of the biggest revolutions in the management of SBS came about in 1980, when Bianchi reported the longitudinal intestinal lengthening procedure which doubled the length of the original segment (fig. 1) [60]. Anatomic variations of the blood supply, such as predominant blood supply to one side of the intestinal wall, limit the potential success of the procedure [61]. Hence, an account of the vascular pattern should always be taken into consideration before splitting the mesentery and transecting the bowel. Various modifications of the Bianchi procedure include using cautery and sutures to minimize stapler-associated leaks and bleeding [62] and oblique stapler application at the proximal and distal ends of the dilated small bowel to obviate the need for complete bowel division, creating a single hand-sewn anastomosis and thus eliminating potential sites of leak or stricture with two anastomoses [63]. Anatomic criteria suggested for patient selection for LILT include i) intestinal diameter > 3 cm, ii) length of residual small bowel > 40 cm, and iii) length of dilated bowel > 20 cm [64].

Fig. 1

Bianchi LILT. A Separating the two leaves of the mesentery carrying blood supply to half of the circumference of the bowel. B Creating a mesenteric tunnel for division of the dilated bowel. C, D Division of the dilated bowel with a surgical stapler into two separate pieces, one-half the size of the original dilated loop. E The two bowel loops are then anastomosed together in an isoperistaltic manner. (Reproduced with permission from [60].)

Fig. 1

Bianchi LILT. A Separating the two leaves of the mesentery carrying blood supply to half of the circumference of the bowel. B Creating a mesenteric tunnel for division of the dilated bowel. C, D Division of the dilated bowel with a surgical stapler into two separate pieces, one-half the size of the original dilated loop. E The two bowel loops are then anastomosed together in an isoperistaltic manner. (Reproduced with permission from [60].)

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However, others suggest that regardless of the bowel length, intestinal lengthening procedures are indicated with life-threatening complications of PN or when substantial bowel dilatation occurs with intestinal failure [65].

In the event the bowel mesentery is unavailable for splitting due to adhesions from previous surgeries or when the short gut consists of only the dilated duodenum, the Iowa two-step elongation procedure, another modification, seems more appropriate than LILT [66]. Here, the bowel is initially connected to a host organ, such as liver [66], abdominal wall [67], or adjacent bowel [68], to allow vessel collaterals to grow into the attached bowel segment, following which the bowel is lengthened with a longitudinal split followed by isoperistaltic anastomosis of the resulting new bowel loops. Since this method requires multiple laparotomies with several weeks of time between surgeries to enable parasitization of the blood supply, it failed to find widespread application.

A review of worldwide published series of LILT revealed varying results with an overall survival ranging from 30 to 100%, and the ability to wean from PN as 28-100% [35, 69, 70, 71]. Early reports of the LILT showed a high complication rate with anastomotic stenosis, staple line leakage, interloop abscess and fistulae formation, and hemiloop necrosis resulting from vascular compromise [35, 72], but with more experience the complication rate has been reduced [70]. LILT is a technically difficult procedure with disadvantages including the necessity for uniform dilatation of the segment to be lengthened and occurrence of recurrent dilatation necessitating additional surgeries. This procedure is a one-time surgery which cannot be repeated on the same intestinal segment, as the vasculature within the mesentery is not further dissectable; however, LILT is definitely feasible after a prior STEP [73].

In 2003, STEP, a simpler technique of bowel lengthening, was introduced by Kim to limit dilatation with minimal risk of intestinal ischemia and in the absence of uniform dilatation over a longer segment (fig. 2) [74]. STEP was first clinically applied to dilated bowel following a Bianchi LILT [75]. From the technical perspective STEP has many clear advantages over LILT as it is easily reproducible, precludes the need of an anastomosis, requires minimal mesenteric dissection, reducing the chance of vascular compromises, and above all it can be performed primarily or repeatedly in patients who develop redilation of their bowel after a LILT or STEP procedure [76, 77]. Asymmetrical bowel dilatations in the short bowel consisting of intricate intestinal segments such as the duodenum and adjacent jejunum are better served with STEP than LILT [74]. STEP has also shown promising results as a primary procedure in neonates with intestinal atresia and marginal length [78, 79]. Problematic bacterial overgrowth including D-lactic acidosis has been better handled with a STEP procedure since, besides reducing stasis and increasing carbohydrate and fat absorption, it decreases the overall bacterial load, thus reducing the amount of carbohydrate substrate available for D-lactic acid production [80].

Fig. 2

STEP: Serial transverse application of a linear stapler, on alternate sides' midway between the mesenteric and anti-mesenteric border, creating a ‘zig-zag' longer, narrower intestinal channel which straightens over a period of time. (Reproduced with permission from [132].)

Fig. 2

STEP: Serial transverse application of a linear stapler, on alternate sides' midway between the mesenteric and anti-mesenteric border, creating a ‘zig-zag' longer, narrower intestinal channel which straightens over a period of time. (Reproduced with permission from [132].)

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Adaptation continues after STEP procedure, requiring on average 1-2 years for noticing significant improvement in intestinal absorption and function. The progress can be gauged by studying various markers like D-xylose [81], a marker of carbohydrate absorption and mucosal integrity, plasma citrulline [82], a marker of small bowel enterocyte mass, and fecal fat content, a marker of intestinal absorptive function. Improvement in intestinal function is secondary to an absolute increase in mucosal absorptive surface area or healing of existing inflamed and atrophic mucosa resulting from stasis and bacterial overgrowth. Intestinal bacterial load also decreases post-STEP, and gradually, with an absolute increase in the surface area, the residual intestine begins to dilate, representing ongoing intestinal adaptation. It takes an average of about 12-24 months for redilatation [83].

However, excessive dilatation may re-invite stasis and bacterial overgrowth resulting in malabsorption, and this prevents achievement of intestinal autonomy in a significant proportion of patients. This is when a repeat STEP or surgical tapering is required [84]. Following a repeat STEP, 13-43% of patients successfully wean off PN regardless of type of initial bowel lengthening [85]. Principles to be followed during repeat STEP include firing of the stapler twice in an alternating fashion between each initial staple line to maintain the intestinal continuity, avoiding the creation of blind ends of bowel, or the other option involves single stapler application between each initial staple line resulting in several blind ends that ultimately need resection [86]. To ensure good blood supply, the staple firings should be applied in a sufficiently dilated segment of bowel which may be difficult due to the asymmetric bowel dilatation after the primary STEP [87].

In order to better track STEP outcomes worldwide, a web-based International Data Registry for patients undergoing STEP was established at www.stepoperation.org.

The choice for one of both surgical lengthening options is essentially driven by feasibility of the procedures and the associated outcome. A Bianchi is the preferred initial surgical option for lengthening, enabling a STEP to be performed at a later date once recurrent dilation occurs. Similarly, the STEP procedure is the better choice when patients have foreshortened mesentery or prior surgeries without preservation of both leaves of the mesentery [74, 88]. Since higher failure and mortality rates have been reported with LILT in shorter remnant intestinal segments, STEP should be the indicated lengthening procedure for dilated segments shorter than 20 cm [89].

Both LILT and STEP are comparable procedures without any obvious advantages over each other. The rate of total PN weaning is more or less similar in both but STEP enables rapid wean of total PN due to its ability to increase the final length to more than 100% of the original length in contrast to Bianchi LILT, where the original length is only doubled [88].

Earlier procedures designed to delay intestinal transit included artificial valves, recycling loops and pouches, and intestinal pacing [35]. Outcomes with these procedures have not been uniformly successful and as such they are only of historical significance. Interestingly, intussusception valve, created by the eversion technique similar to creating an ileostomy, found a role in dilating short segments of bowel by partial mechanical obstruction, subsequently allowing intestinal lengthening procedures [90]. However, since valuable small bowel length is sacrificed in valve construction and subsequent uncontrollable bowel obstruction may demand valve removal, the procedure failed to gain popularity [35].

All available literature suggests that no single AGIR technique offers a rapid guaranteed cure for intestinal failure without any potential complications. Attempts to achieve enteral autonomy are generally better with longer bowel lengths and a greater initial absorptive capability [88]. End-stage liver failure is a clear contraindication for AGIR and necessitates transplantation; hence, bowel lengthening procedures should be performed before the development of liver disease in SBS patients [91]. The role of surgical rehabilitation is to obviate the need for intestinal transplantation but when it fails to generate adequate bowel length for a healthy, disease-free survival, AGIR serves as a bridge to intestinal transplantation [92].

Over the years, small bowel transplantation has emerged as a curative alternative in patients with intestinal failure enabling reduction in PN-associated complications and providing an improved quality of life with better nutrition. The main goal of intestinal transplantation is the restoration of enteral nutrition. Up to 90% of patients undergoing intestinal transplantation can be free of PN [32].

Following the initial pioneering work by Alexis Carrell in the 20th century and animal experiments by Lillehei in 1959 [93], the first clinical transplants were performed in pediatric patients in Boston in 1964 [94]. The initial attempts failed due to technical complications and lack of effective immunosuppressive regimens [95, 96]. The first successful multivisceral transplantation with survival was reported by Thomas Starzl et al. [97] in 1987, followed by Goulet et al. [98] reporting the first successful isolated small bowel transplant with long-term survival, and Grant et al. [99] reporting the first combined transplantation of liver and small bowel in 1989.

Further remarkable improvements in patient and graft survival have been attributed to technical improvements, novel immunosuppressive agents, better understanding of the immune and gastrointestinal physiology, significant advances in anesthesia and critical care, and an overall increase in clinical program experience [100, 101, 102].

The major revolution in intestinal transplantation came when the Center for Medicare and Medicaid Services (CMS) accepted bowel transplant as the standard of care for intestinal failure patients failing PN and other medical or surgical rehabilitation attempts, and offered insurance coverage for the procedure [103].

Currently, small bowel transplantation is offered to SBS individuals who experience PN failure including recurrent catheter-related infections (more than two per year, fungemia, shock, acute respiratory distress syndrome (ARDS)), thrombosis of two of the six major central venous accesses, alterations of growth and development in children, severe dehydration with refractory electrolyte changes, and impending liver failure or established liver disease with cirrhosis and portal hypertension [104]. Further indications also include treatment of motility disorders like total intestinal aganglionosis and microvillus inclusion disease, gastrointestinal neoplastic syndromes involving the celiac or mesenteric roots like desmoid tumors and well differentiated neuroendocrine tumors, and enterocyte deficiencies such as USBS with residual small intestine <10 cm in infants and <20 cm in adults [105, 106]. When SBS results from certain abdominal catastrophes like extensive abdominal trauma, extensive intestinal resection, multiple enterocutaneous fistulas, or chronic diffuse mesenteric vascular thrombosis, complete replacement of all organs of the abdominal cavity (multivisceral transplantation (MVTx)) is required to reestablish normal physiology [107]. Multivisceral transplantation is also indicated with complex portal mesenteric system thrombosis [108], even in the absence of liver or intestinal failure, but more commonly in the context of liver transplantation with complete portal vein thrombosis extending into the superior mesenteric vein (grade III/IV per Yerdel classification) [109].

There is now an emerging philosophy of earlier intervention, with encouraging results reported in transplants being performed at an earlier stage [110] justified by the higher mortality faced by IFALD patients awaiting combined liver/intestinal transplantation [111].

Intestinal transplantation has several variants depending on concomitant other organ failure needing replacement simultaneously with the intestines. Isolated intestinal transplantation (SBTx) is indicated in irreversible intestinal failure in the absence of associated severe liver dysfunction as proven by a liver biopsy (fig. 3). The graft may come from a cadaveric or a living donor. Perfect size match or size reduction, to transplant a segment of 200 cm, is required to enable abdomen closure [112]. The combined liver-intestinal transplantation (SB-LTx) is indicated when intestinal failure patients have coexisting irreversible liver disease. Here, the liver can be transplanted separately or in continuity with the bowel, en bloc with the pancreaticoduodenal arc, via the Omaha technique in which biliary reconstruction is avoided as the donor duodenum serves as a conduit for biliary and pancreatic secretions from the graft (fig. 4). MVTx involves removal and replacement of both native foregut and midgut. The graft may include liver, kidneys, and large intestine depending on the need (fig. 5). In all these transplants, enterostomy of the distal graft ileum is performed to serve for graft surveillance through repeated biopsies assessing allograft rejection.

Fig. 3

Isolated intestinal transplantation: The entire jejunum and ileum is transplanted with or without the colon maintaining as much functional native bowel as possible. The arterial inflow is through an anastomosis between the graft superior mesenteric artery and the native aorta whereas the venous drainage is established into the inferior vena cava or the mesenteric portal system (as shown) through the graft superior mesenteric vein (transplanted organs are shaded). (Reproduced with permission from [32].)

Fig. 3

Isolated intestinal transplantation: The entire jejunum and ileum is transplanted with or without the colon maintaining as much functional native bowel as possible. The arterial inflow is through an anastomosis between the graft superior mesenteric artery and the native aorta whereas the venous drainage is established into the inferior vena cava or the mesenteric portal system (as shown) through the graft superior mesenteric vein (transplanted organs are shaded). (Reproduced with permission from [32].)

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Fig. 4

Combined liver-intestinal transplantation: The liver is transplanted en bloc with the small bowel, arterial supply is established through the superior mesenteric artery and celiac trunk graft through a conduit to the aorta, and venous drainage is made through the hepatic veins to the inferior vena cava. The venous drainage of the native viscera is established through a native portocaval shunt. The upper gastrointestinal continuity is maintained through the native stomach and pancreaticoduodenal complex which are retained and anastomosed to the transplant jejunum (transplanted organs are shaded). (Reproduced with permission from [32].)

Fig. 4

Combined liver-intestinal transplantation: The liver is transplanted en bloc with the small bowel, arterial supply is established through the superior mesenteric artery and celiac trunk graft through a conduit to the aorta, and venous drainage is made through the hepatic veins to the inferior vena cava. The venous drainage of the native viscera is established through a native portocaval shunt. The upper gastrointestinal continuity is maintained through the native stomach and pancreaticoduodenal complex which are retained and anastomosed to the transplant jejunum (transplanted organs are shaded). (Reproduced with permission from [32].)

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Fig. 5

Multivisceral transplantation: The native abdominal viscera is resected and the composite graft, including the liver, stomach, pancreaticoduodenal complex, and small intestine, are transplanted en bloc. The arterial supply is established through the superior mesenteric artery and celiac trunk graft through a conduit to the aorta and venous drainage through the hepatic veins to the inferior vena cava, when the liver is included (as shown) and through the graft portal vein to the cava when recipient liver is retained. The gut continuity is restored by anastomosing the esophagus or gastric remnant with the stomach graft (transplanted organs are shaded). (Reproduced with permission from [32].)

Fig. 5

Multivisceral transplantation: The native abdominal viscera is resected and the composite graft, including the liver, stomach, pancreaticoduodenal complex, and small intestine, are transplanted en bloc. The arterial supply is established through the superior mesenteric artery and celiac trunk graft through a conduit to the aorta and venous drainage through the hepatic veins to the inferior vena cava, when the liver is included (as shown) and through the graft portal vein to the cava when recipient liver is retained. The gut continuity is restored by anastomosing the esophagus or gastric remnant with the stomach graft (transplanted organs are shaded). (Reproduced with permission from [32].)

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Intestinal rehabilitation plays an important role in adaptation post transplantation since grafts may have varying degrees of failure resulting in compromised tolerance to enteral feeding due to anatomical and functional changes induced by ischemia-reperfusion injury, denervation, absence of lymphatic drainage of the allograft, and rejection episodes [113, 114]. Initial nutrition is provided through PN with gradual transition to enteral diet comprising elemental or polymeric formulas when the graft shows signs of function [115]. A low-fat or low-long-chain triglyceride diet is sometimes preferred to reduce the risk of chylous ascites [116].

In children, a SB-LTx is the leading type of transplantation (50%), followed by the isolated SBTx (37%) and the MVTx (13%). In adults, transplantation of the intestine alone is usually performed (55%), followed by the MVTx (24%) and the SB-LTx combination (21%) [32]. Isolated SBTx is increasing in frequency and now exceeds the number of combined liver and intestine transplants which used to be performed more commonly [117]. Recent data from the international Intestinal Transplant Registry (ITR) and Scientific Registry of Transplant Recipients (SRTR) annual report have documented significant improvement in the patient and graft survival following intestinal transplantation in the last decade [118, 119].

For patients undergoing intestinal transplant in 2007, 1-and 5-year graft survival was 69.2 and 53.8%, respectively, for recipients <18 years, and 74.2 and 48.3%, respectively, for recipients >18 years or older. 1- and 5-year graft survival was 74.6 and 48.0%, respectively, among SBTx recipients, and 68.6 and 53.7%, respectively, among SB-LTx recipients. Considering both recipient age and organ transplanted, adult recipients of intestinal transplants have the best 1-year graft survival (79.6%), and pediatric recipients of intestine-liver transplants have the best 5-year graft survival (56.3%) [117]. A significant decline in graft survival over the long term results from infections, malignancy, and chronic rejection [120].

Controversies regarding the inclusion of the colon due to the risk of infection have been challenged with recent reports from few single center series documenting benefits of continence and reduced incidence of dehydration with increased water absorption [121, 122]. Similarly, immunologic benefits, with inclusion of the spleen, in the pediatric population have been documented without altering the incidence of graft versus host disease [123]. Innovative techniques to deal with lack of space and difficult abdominal closure when loss of domain exists include transplantation of full-thickness abdominal wall [124] or vascularized [125] or non-vascularized rectus fascia [126] along with the intestinal allograft, reconstruction of the abdominal wall with acellular dermal matrix [127], and staged abdominal wall closure [128].

In some cases where there has been rapid progression of liver disease with preserved venous access and intestinal autonomy is possible, replacing the liver alone has been beneficial. Certain criteria were proposed by Dell-Olio et al. [129] for the success of isolated liver transplant (iLTx) in patients with intestinal failure which include i) established IFALD (serum bilirubin > 200 mmol/l, moderate/severe fibrosis, portal hypertension), ii) at least 50 cm of remnant functional small bowel in the absence of ICV or 30 cm with ICV, iii) enteral tolerance of at least 50% of the estimated daily energy requirement with an associated increase in weight for a few weeks before the development of IFALD, and iv) no history of recurrent line infections in the presence of dilated dysmotile bowel. Increased organ availability from a cadaveric split liver or a living donor makes this option very attractive. Advantages include cure of portal hypertension resulting in better utilization of nutrients. Further AGIR can also be performed post transplantation to reach enteral autonomy [31, 130, 131]. Despite the reported benefits, iLTx should not become the standard of care but should rather be considered with extreme caution in children with SBS and IFALD. Nutritional outcomes should be followed closely to determine the need for additional AGIR surgeries or intestinal transplantation in the long term.

Management of intestinal failure resulting from SBS continues to be a huge challenge. The potential benefits of both AGIR and intestinal transplantation in surgical management of short gut are now well evident. AGIR procedures offer less complicated and inexpensive techniques of achieving enteral autonomy using one's own bowel. Although intestinal transplantation has demonstrated a clear life-saving role in managing life-threatening intestinal failure, its benefits are limited by organ availability as well as significant financial and physical implications. However, best patient outcomes can be achieved through an individualized plan and a multidisciplinary approach with expertise available at an intestinal rehabilitation center.

The author does not have any conflicts of interest regarding this article.

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