Definition and pathogenesis

Short bowel syndrome (SBS) is often defined as that symptom complex which occurs in adults who have less than 200 centimeters of combined jejunum-ileum following small bowel resection. The syndrome is characterized by diarrhea, weight loss, dehydration, malnutrition, and malabsorption of macro- and micronutrients. Note that some patients who have had extensive bowel resections leaving them with more than 200 centimeters of small intestine can develop symptoms indistinguishable from those who fulfill the technical criteria for SBS. This situation occurs when the remaining bowel is diseased as, for example, in patients with Crohn's disease or radiation enteritis. These latter patients are generally managed like the standard SBS patient.

Extensive small bowel resection occurs under the following circumstances: ischemic necrosis, traumatic injury, severe inflammatory disease and iatrogenic. Any process that results in prolonged obstruction of the superior mesenteric artery or vein, or their major tributaries, can result in ischemic necrosis of the small bowel. This occurs, for example, in patients who suffer a superior mesenteric artery embolus, a superior mesenteric vein thrombosis or a small bowel volvulus. Alternatively, multiple gun shot or stab wounds or blunt trauma to the abdomen may injure several bowel loops. Thus, direct traumatic damage to the small bowel wall without injury to the major vessels may also necessitate extensive intestinal resection. Adult patients may suffer from severe inflammatory processes of the bowel (e.g., Crohn's disease) that may require repeated intestinal resections or they may have severe radiation enteritis which results in SBS. Finally, there may be iatrogenic causes of SBS such as resections of intra-abdominal tumors necessitating concurrent removal of large sections of small bowel or a surgical complication in which the mesenteric vessels are inadvertently but irreparably damaged.

The proportion of patients who fall into one of the above categories depends largely on the specialization of physician who reports a SBS series of patients. Hence, some series indicate that tumor resection with radiation enteritis is the most frequent cause of SBS (3), while others suggest mesenteric infarction (4) or Crohn's disease (5) as the most frequent. Generally speaking, however, SBS in adults commonly occurs as a result of mesenteric infarction/bowel volvulus, Crohn's disease, tumor resection with radiation enteritis, or trauma.

Initial treatment and nutritional management

The immediate perioperative period in those with SBS focuses on resuscitation, stabilization, and diagnosis and treatment of any complications. Patients should be aggressively rehydrated, as many patients with catastrophic bowel events are hypovolemic. Most of these patients are also at risk of sepsis, if not already frankly septic, and therefore require broad spectrum antibiotic coverage. Proton pump inhibitors or H₂ blockers should be started to reduce gastric hypersecretion (6, 7). From a surgical standpoint, every effort should be made to preserve as much bowel as possible, including the ileocecal valve. In addition, if technically feasible in the stable patient and if not done at the initial operative procedure, it is recommended that complete small and large bowel continuity be established in the early postoperative period (2 to 8 weeks) in those with more than 33% of residual colon (Grade A, B, C). Placing all of the intestine incontinuity, including colon, maximizes exposure of all viable intestinal mucosa to enteral nutrients. This enhances optimal adaptation, maximizes absorption, may minimize complications, and improves the chance that the patient will become independent of intravenous nutrition in the future (i.e., “nutritional autonomy”). Several studies indicate a correlation between recovery from SBS and the length of residual bowel, presence of ileocecal valve, and presence of colon in continuity (3, 4, 8, 9).

Total parenteral nutrition (TPN) is often needed on a prolonged or permanent basis in the management of SBS patients. Its main purpose is to support the SBS patient while intestinal adaptation takes place and specific treatment is instituted. TPN should be provided on only 3 to 4 nights each week to limit appetite suppression. In addition, “cycling” the TPN may reduce the risk of TPN-associated liver dysfunction. Hydration fluid can be provided on the other nights if clinically indicated. At times, however, caloric requirements necessitate TPN delivery on 6 to 7 nights per week (Grade C) (10).

Specific treatment of SBS includes antimotility agents (e.g., loperamide and diphenoxylate) which slow intestinal transit time and allow increased absorption of nutrients and fluid. Some food intake is desirable in the subacute postoperative period to enhance intestinal adaptation and minimize intestinal atrophy. However, diarrhea can be limited by initially restricting food and fluid consumption to 600 kcal/day and 600 ml/day respectively. As patients progress to the chronic phase of SBS, intestinal adaptation continues over 12 to 18 months and the absorptive capacity of the residual bowel improves significantly. During this time, the patient should increase caloric and fluid intake as allowed by stool output. It is recommended that the diet in those with colon in continuity should be high in complex carbohydrates (60%) and protein (20%) and low in fat (20%). In those without colon, a more liberal intake of fat with decreased carbohydrate intake may be desired as the decrease in carbohydrate intake may reduce fluid losses from osmotic diarrhea. Fluid should be an isotonic, electrolyte containing solution which will enhance fluid absorption and minimize osmotic diarrhea (Grade A and C) (4, 8, 10–13).

Growth factors

In individuals with healthy remnant bowel who receive the “standard” supportive care and treatment as described above, a minimum of 110–150 cm of small bowel is required to achieve nutritional autonomy if there is no colon in continuity, and 50–70 cm of small bowel if a portion of colon remains in continuity with the small bowel (8). This leaves are large group of individuals who may never become TPN-independent if other treatments are not instituted. Animal research suggests that growth factors and specific nutrients enhance intestinal adaptation and thus may increase the chances of nutritional autonomy in SBS patients with very short segments of bowel. Only a limited number of studies have been done in humans in this regard and the largest clinical studies have focused on the efficacy of growth hormone (GH) and glutamine (GLN) (4, 5, 8, 14–16).

A combined approach of GH and GLN administration was used in forty seven SBS patients in conjunction with a diet high in complex carbohydrates (60%) and protein (20%) and low in fat (20%) (14). Forty three of the forty seven patients had a portion of colon in continuity with the remnant small bowel and a median jejunal-ileal length of 50 cm. The remaining four patients were without colon and had a median jejunalileal length of 102 cm. All were TPN dependent. After a twenty-eight day treatment period (GH 0.10–0.14 mg/kg/day SQ and GLN 30 g per day) and with an average one year follow-up, 40% of the patients achieved complete nutritional autonomy, and an additional 40% had a significant reduction in TPN dependence. Since these initial studies, approximately 225 SBS patients have been treated with the combined GH, GLN, modified diet protocol. Long term follow-up of these patients still demonstrates that 40% of patients achieve nutritional autonomy and 40% have a significant reduction in TPN-dependence (4). Based on this information, it is recommended that patients be considered for GH and GLN therapy if they have very short segments of bowel or have failed to respond to standard therapy (Grade C). Table I presents data of a typical patient receiving this treatment who has 102 cm of jejunum-ileum ending in an ostomy as a result of multiple bowel resections for treatment of Crohn's disease.

Table I

Clinical Indices of Patient “A” prior to and just after 26 days of treatment with Growth Hormone, Glutamine, and Diet modification.

Surgical treatments and intestinal transplantation

Surgical therapy of SBS falls into two categories: those procedures designed to prolong intestinal transit time and those designed to increase functional intestinal absorptive surface area including intestinal transplantation. To prolong transit time, surgeons have created intestinal valves and sphincters using various techniques; reversed segments of small and large bowel and anastomosed them in continuity with the small bowel to serve as a antiperistaltic segment; created recirculating loops and pouches; and have attempted retrograde intestinal pacing. Those with experience with the procedures conclude that “operations aimed at prolonging intestinal transit time are especially inconsistent” (3). In addition, since these procedures have significant complications, it is recommended that they not be used on a routine basis (Grade C).

In contrast, non-transplant procedures designed to increase functional absorptive capacity of the bowel can be quite successful in the appropriately selected individual with dilated bowel. These procedures include stricturoplasty for those with a stricture, and tapering enteroplasty with or without intestinal lengthening. Though the actual surface area of intestinal mucosa is not increased with these procedures (at least acutely), the function of the bowel improves and thus absorptive capacity can increase significantly. At least one series suggests that these procedures can lead to nutritional autonomy in 70% of patients and have significant improvement in intestinal function in 90% of patients (3). Thus, it is recommended that in SBS patients who have a defined surgical problem, such as a stricture or poorly functioning dilated segment, be considered for one of these procedures (Grade C).

Intestinal transplantation is also a consideration in SBS patients who have failed more conservative approaches to treatment. The international experience with transplantation was recently reviewed by Grant (17). He analyzed the results of 180 transplants in 170 patients including intestine alone, bowel/liver, and multivisceral transplants. The results are present in Table II and indicate a high morbidity (50%) but with a significant proportion of patients achieving nutritional autonomy (40%). Hence, it is recommended that intestinal transplantation be reserved for those who have failed other treatment options and have developed life-threatening complications related to TPN (Grade C). Future advances in the management of immunosuppression of these patients may make this a more attractive alternative for others with SBS.

Table II

Results of intestinal transplantation at three years (17).

Designing a treatment plan based on predicted outcome

All therapies of SBS have inherent difficulties and their associated complications. Hence, it is important to design a treatment program based on that which is likely to achieve nutritional autonomy with the least risk. As the initial step in planning therapy and assessing prognosis in SBS, it is important that the length of jejunum-ileum and per cent of colon remaining be documented at the time of bowel resection. Because of problems associated with determining the exact length of pre-existing small bowel, it is best to estimate the length of residual small bowel in absolute terms (i.e., centimeters remaining) rather than relative terms (i.e., percent remaining). This is done by measuring the small bowel with minimal tension along the anti-mesenteric border starting at the ligament of Treitz and continuing to the end of the small intestine. In contrast, if the colon is also resected, an approximation of the per cent of colon remaining should be estimated and recorded. Based on the residual small and large bowel length, a treatment plan can be developed and likelihood of achieving nutritional autonomy predicted.

Adults with SBS usually weigh 50–75 kg and previous studies using standard treatments suggest a bowel length of approximately 50 to 70 cm anastomosed to colon is required for SBS to become independent from TPN (8). This corresponds to a bowel length to body weight ratio of 1.0 cm/kg and suggests that patients with such a ratio may not require specialized medical treatment beyond standard therapy and support with TPN. Patients with segments of small bowel that are shorter may be tried on a regimen of GH and GLN assuming surgically defined problems with strictured or dilated bowel have been corrected. Patient's with an small intestinal length to body weight ratio from 0.5 to 1.0 have a high probability (80%) of achieving independence from TPN with this specialized treatment. Patients with a ratio between 0.25 and 0.5 have a lesser probability (50%) of responding. Finally, patients with a ratio less than 0.25 have a low probability of responding to this therapy and such patients should be considered for other interventions such as intestinal transplantation (see figure 1) (8). Predictive factors for successful outcomes can be determined for adult patients without colons for this and other treatments.

Figure 1

Probability of achieving nutritional autonomy with “standard therapy” or treatment with growth hormone (GH), glutamine (GLN) and a modified diet based on patient weight and jejunalileal length. Figure is based on results from 45 short (more...)

Conclusion

Significant progress has been made in the support and treatment of patients with short bowel syndrome. It is currently estimated that SBS patients have a one year survival that approaches 75% as opposed to a 20% one year survival reported by Haymond in 1935 (2, 9). Principles that increase the chance of achieving complete nutritional autonomy include resection of as little bowel as possible, preservation of the ileocecal valve, and placement of all the remaining small bowel and colon in continuity (if possible) at the initial or later procedure. Enteral feeding of whole food should be encouraged to enhance intestinal adaptation even if TPN is required. Well defined problems that develop later, such as intestinal strictures or dilated, poorly functioning bowel should be corrected surgically. Patients that remain TPN-dependent after these measures should be considered for growth factor therapy such as administration of growth hormone and glutamine. Finally, patients who remain TPN-dependent with life-threatening problem despite the above efforts should be referred for possible intestinal transplantation. Future benefits in the management of the patients will possibly be achieved with the introduction of new, more potent growth factors (e.g., glucagon-like peptide 2) and improvement in adjunctive therapies in intestinal transplantation.

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