Short bowel syndrome

Over the last 3 decades, there has been significant improvement in the survival and quality of life of patients who require home parenteral nutrition; however, parenteral nutrition remains costly, is associated with multiple complications, and does not promote the function of the remaining bowel. Intestinal rehabilitation refers to the process of restoring enteral autonomy and decreasing dependence on parenteral nutrition by utilizing dietary, pharmacological, and, occasionally, surgical interventions. A major focus of research has been to identify a trophic factor that will enhance adaptation of the remaining gastrointestinal tract following massive gut resection and allow enteral autonomy. Whether intestinal rehabilitation occurs as the result of increased intestinal adaptation or as the result of a comprehensive approach to care has yet to be determined. This article reviews intestinal failure as the result of short-bowel syndrome and the management strategy of an intestinal rehabilitation program in the care of these patients. (Progress in Transplantation. 2004;14:290-298)

Notice to CE enrollees:

A closed-book, multiple-choice examination following this article tests your ability to accomplish the following objectives:

1. Discuss the physiological abnormalities associated with short-bowel syndrome

2. Identify important parameters in assessing the patient with short-bowel syndrome

3. Describe considerations for the diet and fluid plan for the patient with short-bowel syndrome

4. Review pharmacological and surgical strategies for management of short-bowel syndrome

Before the development of total parenteral nutrition in 1968, the medical community had little to offer a patient with intestinal failure due to short bowel syndrome.1,2

Intestinal failure (IF) is commonly defined as any intestinal condition that requires the use of parenteral support to maintain nutritional and hydrational balance. A child who cannot grow without intravenous support would also be characterized as having IF.3 IF may be acute or chronic, and occurs in general because of inadequate intestinal length or function (Table 1). The most common cause of IF is short-bowel syndrome (SBS), which results from massive intestinal resection and usually occurs in the setting of Crohn disease, mesenteric vascular events, necrotizing enterocolitis, congenital intestinal anomalies, or trauma.4 The incidence and prevalence of SBS remain poorly understood, with previous estimates being extrapolated from the number of patients on home parenteral nutrition (PN) because SBS is the most common reason for requiring home PN.4 However, these numbers do not account for patients with SBS who never received home PN or were successfully weaned from PN.

Short-Bowel Syndrome

In adults, SBS can be defined as the presence of less than 200 cm of small intestine. The normal length of intestine in an adult is considered to be 300 to 800 cm.4 In infants, the diagnosis of SBS relies less on an anatomical definition and more on a functional one, as the amount of resection required to produce malabsorption varies with factors such as age, the presence or absence of an ileocecal valve, and length of residual colon.45 The full-term neonate has approximately 240 cm of small bowel and 40 cm of colon; however, the length of the jejunum, ileum, and colon doubles in the last trimester of pregnancy making the gestational age an important determinant of bowel length.6

Establishing an accurate estimation of bowel length and anatomy is important to optimize the care of the SBS patient, but is often difficult. Although information from operative reports is preferred, such notes frequently record the amount of bowel removed rather than the amount remaining. A barium contrast small bowel series may also provide an estimate of bowel length and is useful to delineate other structural features such as the bowel diameter. Frequently, a combination of these 2 methods is used. When considering small bowel length, the duodenum is generally not included and measurements begin at the ligament of Treitz.

Anatomical factors that affect the outcome of SBS patients include not only the length and region of the remaining small intestine but also the presence of the colon. In general, an SBS patient will have I of the following bowel anatomies: jejuno-colic anastomosis, end-jejunostomy, or jejuno-ileal anastomosis. Patients with a jejuno-colic anastomosis rarely have an ileocecal valve. Patients with a jejuno-ileal anastomosis have the best prognosis; however, this anatomy is the least common. Patients with an end-jejunostomy are the most difficult to manage and are most likely to require permanent parenteral support.7 In adults, at least 50 cm of small bowel in continuity with the colon or 120 cm of small bowel without colon is considered necessary to allow autonomy from PN.8,9

Intestinal Adaptation

Following massive intestinal resection, a process known as intestinal adaptation occurs in which the remaining bowel undergoes a variety of macroscopic and microscopic changes to increase its ability to absorb fluid and nutrients.10 Intestinal adaptation can be related to both structural and functional changes. In structural adaptation, the villi increase in size and absorptive surface, whereas functional adaptation refers primarily to a slowing in the rate of transit, allowing increased time for absorption to occur. The degree of bowel adaptation is dependent, in part, on the residual bowel anatomy. The ilcum is capable of both structural and functional adaptation whereas the jejunum mainly adapts functionally. The increased ability of the ileum to adapt is multifactorial and is related to its less permeable mucosa, making concentration of its contents possible; its slower transit time, which allows increased time for absorption; and its ability to absorb bile salts, which improves fat absorption and reduces the effects of these substances on colonie function. As a result of the differences in adaptive abilities between the ileum and the jejunum, a jejunal resection is generally better tolerated.10,11 Unfortunately, in most patients with SBS, the ileum has been resected, leaving only some portion of the jejunum-usually along with a portion of the colon.

Following massive intestinal resection, 3 distinct clinical stages have been described.10 In the first few weeks after resection, significant fluid and electrolyte shifts require copious amounts of intravenous fluids. In the second stage, nutritional support is the primary concern. This stage may last for up to 2 years, and during this time most structural and functional adaptation and most PN weaning occur. Stage 3 is considered a homeostatic phase, in which no further improvement or adaptive changes occur.11,12

Assessment of Patients With Short-Bowel Syndrome

Treatment options for SBS patients include longterm home PN, intestinal rehabilitation, and/or intestinal transplantation. To determine the most appropriate therapy for an individual patient, a comprehensive evaluation is necessary (Table 2). A multidisciplinary approach is preferred and should include educational, emotional, and psychological evaluation and assistance (Table 3). A physician experienced in the care of patients with IF should oversee and guide the evaluation and management of these highly complex patients.

Nutritional Assessment

A nutritional assessment by a dietitian experienced in the care of these patients is important. An estimation of the caloric and hydration needs of the patient is needed to optimize an individualized oral and parenteral nutrition plan.13 In addition, SBS patients are at risk for a variety of micronutrient deficiencies because of physiological changes related to the altered bowel anatomy. For instance, vitamin B^sub 12^ is absorbed in the terminal ileum and should be administered intramuscularly once a month to SBS patients with resections involving greater than 60 cm of the terminal ileum. Fat-soluble vitamin deficiencies, particularly vitamin D, are also common in these patients, as well as zinc and magnesium deficiencies. Consequently, it is important to monitor micronutrient levels periodically and treat deficiencies if they exist.

Venous Access

Determination of patent venous access sites is also important. Although advances in interventional radiologie techniques have improved the ability to gain intravenous access, in general, if an adult on long-term home PN has lost 3 of the 6 major venous access sites or a young child has lost 2 of the 4 standard venous access sites, then referral for small bowel transplantation should be considered.14

Education

To prevent complications from home PN, the patient must become an active participant in his or her healthcare. The patient or a member of the patient's family must be willing to accept this responsibility as long-term nursing care is rarely covered by insurance. Initiating a patient on home PN requires extensive teaching on the method of administration and potential complications (Table 4).15 A knowledge assessment by a clinical nurse specialist can help design an appropriate care plan for the patient. The patient should receive education about the disease process and methods to minimize complications related to the central venous catheter. It is also beneficial to provide information about support groups such as the Oley Foundation to allow the patient to build a network of positive support and an enhanced capacity to live with home PN.15

The availability or a wound care nurse is vaiuaoie in the care of SBS patients with complex wounds, fistulae, and ostomies. It is important to determine how frequently the patient needs to empty the ostomy bag, particularly at night, in order to determine if the patient is receiving adequate rest. In this regard, ostomy appliances exist that make it possible for the patient with high ostomy output to go 6 to 8 hours between bag emptying.

Psychosocial Assessment

The involvement of a psychologist and/or psychiatrist may help identify and manage psychosocial and chronic pain problems that commonly occur in these patients and that can lead to abuse of pain medications and/or rob patients of the energy to cope with their illness. In addition, a social worker is necessary to assist SBS patients who struggle with social and financial stress.

Intestinal Rehabilitation

Intestinal rehabilitation is an attempt to maximize the physiological processes that occur following a massive bowel resection in order to enhance intestinal adaptation and restore enterai autonomy." In addition to patient education and support, an individualized approach to diet, fluid management, medications, and, occasionally, surgery is necessary.

Diet and Fluids

Little experimental evidence relevant to humans regarding the importance of diet in the management of SBS is available, consequently, there is limited consensus on the importance of the oral diet in the management of SBS. Few studies have investigated the effect of a diet program, as opposed to a specific nutrient, on the management of SBS.11 SBS patients differ in their response to dietary manipulation depending on their bowel anatomy; specifically, the presence or absence of a colon. Norgaard and Mortensen16 demonstrated that patients with a colon had better energy absorption on a diet high in carbohydrates compared to a diet high in fat. Conversely, in SBS patients without a colon, the high carbohydrate diet increased ostomy output. Clinical experience confirms the value of diet in the management of SBS. A diet optimized to the needs of the individual patient can reduce stool output, improve energy absorption, and assist in PN weaning.13,17

The diet for a patient with IF should be designed to fit the individual's taste, tolerance, and bowel anatomy.17 Adult SBS patients absorb only one half to two thirds as many calories as normal; therefore, the caloric intake must be increased by at least 50%. The best-tolerated meal pattern is usually 5 to 6 meals spread throughout the day. High-fiber, nutrient-poor foods and highly concentrated sweets should be avoided because both can stimulate diarrhea. In contrast, complex carbohydrates reduce the osmotic load and potentially exert a positive effect on the adaptation process.17 Because the proximal jejunum is rarely resected in SBS patients, lactose is generally well tolerated.18 Oxalate restriction is also important in SBS patients with a colon, as 25% of patients with less than 200 cm of small bowel and a colon develop oxalate nephropathy.19

When tolerance of oral feedings limits PN weaning, the use of enteral tube feeding is another method that may be beneficial to provide additional calories. "Drip feedings" or a continuous rate administered over 12 to 24 hours is generally better tolerated than intermittent bolus feedings because of greater absorption of nutrients and less osmotic diarrhea. In infants and children, small oral feedings are necessary to prevent oral aversion and potential future development of eating disorders.

Fluid management in SBS is also guided by the remaining bowel anatomy. SBS patients with an intact colon generally tolerate hypotonic fluids (eg, water), whereas patients without a colon usually require a glucose-electrolyte solution, also known as an oral rehydration solution (ORS), to minimize stool output. To maximize water and sodium absorption in the jejunum, an ORS with at least 90 mmol/L of sodium is necessary.20 Two to 3 liters sipped throughout the day may be necessary to maintain hydration. Although a variety of affordable commercial products are available, the least expensive is recommended by the World Health Organization and can be prepared by the patient using common kitchen ingredients.21 Although fluid composition is less important in patients with a colon, adequate sodium should be provided. Regardless of bowel anatomy, hyperosmolar fluids should be avoided because they will aggravate stool losses. Patients who experience a bowel movement immediately after eating may benefit from separating their ingestion of fluids and food. Parenteral fluids will be necessary if the stool output exceeds fluid intake despite the use of an ORS and antidiarrheal and antisecretory agents.

Pharmacological Strategies

Medical therapies utilized in an intestinal rehabilitation consist mainly of antimotility and antisecretory agents to control stool losses. These agents improve functional adaptation by improving the absorptive efficiency of the bowel. Most orally administered medication is absorbed in the proximal jejunum. As a result, the majority of SBS patients absorb oral medications, although higher closes may be required to achieve the desired effect. When less than 50 cm of jejunum is present, an intravenous formulation or oral solution may be necessary.

Massive bowel resection is associated with transient gastric hypersecretion, which can result in peptic ulcer disease and impairment of digestive enzymes.22 Histamine type 2 receptor antagonists (eg, ranitidine) and proton-pump inhibitors (eg, lansoprazole, omeprazole) are commonly used in the first year following resection to reduce gastric secretions, thereby resulting in decreased stool losses and acidity.22

Antidiarrheal agents function to reduce intestinal motility; however, they also reduce intestinal secretion to some degree. The most commonly used antidiarrheal agents in clinical practice are loperamide, diphenoxylate, codeine, and tincture of opium. Tincture of opium may be added to enteral feedings and can be titrated with the drip rate, making it simple to use. However, it is quite sedating and expensive, and may be addictive with long-term use.23,24 In a study involving adults,23 loperamide 16 mg daily proved to be more effective than 240 mg codeine daily. However, there may be a synergistic effect when these medications are used together. Diphenoxylate has a similar efficacy to loperamide; however, it also has more central nervous side effects thus limiting its use. To be most effective in SBS, antidiarrheal agents need to be administered in larger doses than usual and should be administered before meals and at bedtime. However, although these antimotilily agents can reduce transit time, in a dilated bowel, they may worsen bacterial overgrowth and exacerbate stool output.

Small bowel bacterial overgrowth (SBBO) occurs commonly in SBS patients and may aggravate stool output and make tolerating an oral diet difficult. The anatomical and physiological changes that occur in SBS together with the medications commonly used foster the development of SBBO.25 Typical symptoms of SBBO include flatulence, malodorous stools, increased stooling, and nausea. As these symptoms are not specific to SBBO, diagnosing SBBO as the cause can be challenging. Upper endoscopy with aspiration of duodenal/jejunal fluid to identify excessive number of bacteria is considered the gold standard in the diagnosis of SBBO, although more than 50% of the bacterial species in the gut are not culturable. The primary noninvasive test to diagnose SBBO is a hydrogen breath test; however, its use in SBS is also limited by a number of factors, most importantly, the definition of "abnormal" in this population.11 Other indicators suggestive of SBBO that are sometimes useful include elevated D-lactate and folate levels, metabolic acidosis, and excessive urine indicans.25 Once the diagnosis of SBBO is established and goals of therapy identified, it is generally treated with broad-spectrum antibiotics. The success of the therapy is determined by the alleviation of the symptoms, decrease in stool output, and/or weight gain. Continuous antibiotic therapy is often needed long term to control the symptoms. In this instance, rotation of different antibiotics should be considered to decrease the risk of antimicrobial resistance. Other measures that may be useful to prevent or treat SBBO include a diet low in carbohydrates (especially for children), probiotics (eg, lactobacillus GG), intermittent gut lavage with polyethylene glycol, prokinetic agents (eg, metoclopramide), and bowel-tapering operations.25-27

Trophic Factors

A number of pharmacological agents including growth hormone, glutamine, and glucagon-like peptide-2 (GLP-2) have been demonstrated to have trophic or growth promoting properties on the intestinal epithelium in animal models of SBS. These encouraging reports have been followed by conflicting reports of efficacy regarding the enhancement of intestinal absorption, adaptation, and PN weaning in humans. Currently, only uncontrolled trials of PN weaning using a combination of growth hormone, glutamine, and optimized diet have been published.13,28-30 In 1995, Byrne et al29 published a case series of 47 patients, most of whom had a colon-in-continuity, treated with the above regimen for 3 weeks followed by continued use of the diet and glutamine. Forty percent of the patients had been weaned from PN and 40% had made significant reductions in their PN over a follow-up period averaging 1 year with the longest follow-up of more than 5 years.29 In 3 subsequent randomized, controlled trials, conflicting data on nutrient absorption have been demonstrated, thus, the efficacy of the combination of growth hormone, glutamine, and optimized diet remains controversial.30-32

Byrne and colleagues33 have recently completed a randomized, controlled, prospective study of the above treatment approach in 41 PN-dependent SBS patients in which PN reduction was the primary end-point. The control group was treated with an optimized diet supplemented with glutamine. A recent report of the preliminary data demonstrated a significant reduction in PN requirements in all groups studied; however, the extent of reduction was greatest in the group in which growth hormone was administered in addition to the diet and glutamine. On the basis of this evidence and the safety of the treatment program, the Food and Drug Administration recently approved the use of growth hormone in patients with SBS on PN as an aid in PN weaning. Although encouraging, further controlled studies investigating the optimal dose, duration, and timing of administration in relation to the onset of SBS are needed before this therapy can be routinely advocated for SBS patients.11

GLP-2 is a peptide secreted from endocrine cells residing within the small and large intestine. A pilot trial in humans with SBS has suggested a benefit in terms of enhancing nutrient absorption.34 Although there are currently no data on its utility in PN weaning, a large, multinational, randomized, controlled trial to study this issue is soon to begin.

Glutamine is a "conditionally essential" amino acid that is a primary energy source for the enterocyte and has been shown to prevent mucosal atrophy and deterioration in gut permeability in patients receiving PN. Glutamine may be administered orally and is well tolerated.35 However, data from 2 small randomized, controlled studies in SBS patients have found no difference in small bowel morphology, gut transit time, nutrient absorption, or stool output related to the use of glutamine.36,37

Surgical Strategies

The majority of patients with SBS will require additional surgery at some point. It is crucial that in subsequent operations as much bowel as possible be preserved and the focus be on maximizing the function of the remaining bowel.38 Surgical interventions utilized to promote intestinal rehabilitation, sometimes referred to as autologous gastrointestinal reconstruction, are designed to improve bowel function and include operations to increase intestinal lengthening (eg, Blanchi procedure) and slow transit (eg, reverse intestinal segment).39 Operations such as these should be considered only when the patient is stable and medical and dietary management has been maximized. The function of the bowel can also be improved by surgeries that restore continuity, relieve obstruction, repair a fistula, and eliminate diseased bowel.39 Although there are encouraging results from case studies, evidence of long-term success has not yet been documented and only a small proportion of SBS patients are candidates for these procedures.

For most patients with SBS and life-threatening complications such as liver disease or loss of venous access sites, intestinal transplantation is the best surgical option.40 Transplant options for SBS patients may include isolated intestinal transplant, combined liver-intestinal transplant, a multivisceral transplant, or in some cases an isolated liver transplant.41 Advances in surgical techniques and immunosuppressive medications have made intestinal transplantation a viable lifesaving alternative. In the future, transplantation may provide a lifestyle alternative to patients who wish to "trade" home PN for immunosuppression; however, currently the 1- and 5-year survival rates are better for patients on well-managed home PN.14,42,43

Conclusion

The care of SBS patients is complex and challenging, requiring a multidisciplinary approach. The physiological changes, referred to as adaptation, which occur in the intestine after surgical resection remain poorly understood. Intestinal rehabilitation is an attempt to maximize the physiological processes that occur following massive bowel resection in order to enhance the intestinal adaptive process and restore enterai autonomy. The goal of an intestinal rehabilitation program is to reduce or eliminate PN requirements by using an individualized plan of dietary, medical, and surgical strategies while simultaneously improving patients' quality of life and longevity and decreasing costs and complications associated with PN. Although there may be no single optimal method, an experienced team, careful clinical assessment, and attention to detail can optimize the chance for success. We advocate a stepwise approach to PN weaning with specific oral calorie and fluid goals in mind and frequent monitoring of food and fluid intake and stool and urine output to guide PN weaning decisions. Regular monitoring of electrolyte and micronutrient levels is important during the weaning process. There is currently insufficient evidence to support the routine clinical use of trophic factors as an aid to PN weaning. Autologous gastrointestinal reconstruction and intestinal transplantation remain promising treatments for the appropriate candidate. Because of the complexities of the care of SBS patients, consideration should be given to referring these patients to an experienced center that can provide a comprehensive range of services.

PROGRESS IN TRANSPLANTATION

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PROGRESS IN TRANSPLANTATION courses are approved by AACN and the North American Transplant Coordinators Organization (NATCO). AACN is accredited as a provider of continuing education in nursing by the American Nurses Credentialing Center's Commission on Accreditation. AACN programs are approved by the State Board of Nursing of Alabama (#ABNP0062), California (01036), Florida (#FBN2464), Iowa (#332), Louisiana (#ABN12), Nevada, and Colorado. AACN programming meets the standards for most other states requiring mandatory continuing education credit for relicensure. NATCO is an approved provider of continuing education by the American Board of Transplant Coordinators. ABTC has approved this educational offering and grants Continuing Education Points for Transplant Coordinators under NATCO approved provider #4000.

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Cindy R. Brown, APRN, NP-C,

John K. DiBaise, MD

Departments of Surgery and Internal Medicine, University of Nebraska Medical Center, Omaha, Neb

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