TEMAS DE REVISIÓN

Nutritional considerations and management of short bowel syndrome

José Saavedra*

RESUMEN

Pocas condiciones plantean un reto tan grande, en lo que se refiere a soporte nutricional prolongado, como el síndrome de intestino corto (SIC). A pesar de lo complejo que es el cuidado de estos niños, el gran avance en el pronóstico y mejoría clínica que ha ocurrido en las últimas décadas, en gran medida se debe al avance en lo que significa nutrición entéral y parenteral. La mayoría de niños desarrollan normalmente mientras ocurre la adaptación intestinal. La presente revisión hace énfasis en las consecuencias nutricionales de una malabsorción severa, los problemas clínicos que tienen influencia en el estado nutricional y recomendaciones nutricionales en la nutrición enteral y parenteral. Igualmente se enfatiza en la importancia que tiene en hacer esfuerzos persistentes y agresivos con nutrición enteral como terapia primaria para estimular la adaptación intestinal y minimizar las complicaciones.

PALABRAS CLAVES: Síndrome de intestino corto en la infancia, malabsorción severa, nutrición parenteral, nutrición enteral

SUMMARY

Few conditions pose as great a challenge, in terms of long term nutritional care, as short bowel syndrome (SBS). Despite the complexity of care which children with SBS require, the great improvement in the prognosis and outcome over the past few decades can be attributed, in great measure, to advancements in both parenteral and enteral nutrition support. Most children can maintain normal growth and development while intestinal adaptation occurs, and ultimately achieve independence from parenteral nutrition. This review focuses on the nutritional consequences of severe malabsorption clinical problems which influence nutritional status, and parenteral and enteral nutritional recommendations. The importance of aggressive and persistant efforts with enteral feeding as a primary therapy to enhance bowel adaptation and tominimize complications is emphasized.

KEY WORDS: Short bowel syndrome, severe malabsorption, parenteral nutrition, enteral children nutrition.

INTRODUCTION:

Advances in nutritional and medical therapies have dramatically changed the outcome for infants and children with short bowel syndrome (SBS) in the past 25 years. Most children who have undergone extensive small bowel resection now achieve normal growth and development and a remarkably good quality of life. Management of nutritional and medical therapies poses a special challenge to the child caregivers and team of health care providers.

Definition

SBS is a malabsorptive disorder that occurs as a result of decreased functional mucosal surface area, usually due to massive resection of the small bowel. The malabsorption of macro and micro nutrients, fluid, and electrolytes may lead to severe undernutrition, fluid, acid/base balance and electrolyte disturbances. Malabsorption may be exacerbated by complications frequently associated with SBS, such as bacterial overgrowth and dysmotility. These problems lead to a host of symptoms including diarrhea, abdominal pain, distension and vomiting. The severity of these disturbances varies with the age of the child, the length and location of the bowel which is removed and the condition of the remaining bowel.

Etiology

The most common causes of SBS in infants include congenital anomalies (jejunal and ileal atresia, gastroschisis); necrotizing enterocolitis; and vascular injury (1-3). Other causes of SBS in infants and children include small bowel resection due to long-segment Hirschsprung's disease, omphalocele, Crohn's disease and trauma. Although rare, congenital short bowel may also be a cause of SBS in a small number of infants. Radiation enteritis may lead to functional SBS if injury to small bowel mucosa is extensive.

The prognosis for children with SBS has improved primarily due to advances in parenteral nutrition and the understanding of the importance of enteral nutrition. Specialized enteral nutrition support is essential to promote intestinal adaptation. The small bowel has a unique capacity for adaptation while sustaining normal growth and nutritional status. The total intestinal length increases as well, from approximately 200 300 cm. at birth in a full- term infant, to approximately 450-700 cm. in the adult (4,5). The intestinal length nearly doubles during latter gestation, which suggests that a short bowel in the pre-term infant may eventually function as well as somewhat longer residual segments in a full- term infant (6). From this point of view, the infant and young child may have a more favorable long-term prognosis that an adult, due to the greater capacity for intestinal growth. Overzealous use of antimotility agents such as loperamide may actually worsen distension and bacterial overgrowth.The capacity for adaptation and eventual ability to absorb all nutrients necessary to sustain growth by the enteral route may not be known for weeks or months following the initial resection as attempts to feed progress.

Now days the most common causes of mortality in children with SBS are chronic parenteral nutrition-associated liver disease or sepsis. The ultimate prognosis for long-term survival depends on intestinal adaptation and the ability to reach full enteral feedings without these complications.

Intestinal adaptation and long-term outcome depends, in part, on the length and location of the residual small intestine. Before the days of adequate nutritional intervention, infants with less than 15 cm of small bowel with the ileocecal valve, or less than 40 cm of small bowel without the ileocecal valve rarely survived (1). The dramatic improvement in prognosis is evident when the earlier experiences are compared with those from the mid -1980's. Dorney and others reported that ultimate survival may be possible with as little as 11 cm of jejunoileum with an ileocecal valve and as little as 25 cm of jejunoileum without an ileocecal valve (7). However, more recently, the prognosis for children with even less residual small bowel without an ileocecal valve has improved. There are case reports of children with as little as 12 cm of residual small bowel without an ileocecal valve who have survived and been successfully weaned from parenteral nutrition support (8). Our experience is similarly positive. We have cared for children with as little as 10 cm. of residual small bowel without an ileocecal valve who where eventually weaned completely from parenteral nutrition by 4 years of age.

Although isolated duodenal resection is uncommon, the removal or bypassing of the duodenum may result in malabsorption of micronutrients and lead to clinically significant deficiencies. Malabsorption of iron, folate and calcium may lead to anemia and osteopenia in the child who had undergone duodenal resection. Malabsorption of fat and lipid-soluble vitamins may occur in the absence of adequate digestion and absorption aided by duodenal pancreatic and biliary secretions.

Extensive jejunal resection often leads to significant carbohydrate malabsorption due to the loss of the primary intestinal site of disaccharidase activity. Undigested and malabsorbed carbohydrate contributes to osmotic diarrhea. The duodenum and jejunum are also the primary site of absorption of proteins, fats copper and lipid-soluble vitamins. Although resection of the ileum and preservation of the jejunum may initially cause fewer complications associated with fluid and nutrient absorption, the long-term capacity for adaptation is greater in the ileum after a proximal small bowel resection than in the jejunum after a distal small bowel resection (9).

Extensive resection of the ileum may lead to severe, early consequences. There may be tremendous fluid and electrolyte malabsorption due to the inability of the jejunum to compensate.

The epithelial junctions of the jejunum are likely to leak fluid even as a large proportion of nutrients are absorbed. Sodium chloride absorption is necessary in order to maintain fluid absorption in the presence of steep concentration gradients. If partial resection of the ileum occurs, and sodium chloride has been absorbed proximally, fluid loss may be compounded by the inability of the remaining ileum to absorb fluid in the presence of a steep concentration gradient created by unabsorbed solutes such as potassium and carbohydrates. High volume watery stool losses are more likely to occur following substantial ileal resection compared with resection of the jejunum.

Bile salt malabsorption following ileal resection may also contribute to watery diarrhea and fat malabsorption. The majority of bile salts are actively absorbed in the terminal ileum by way of a sodium dependent carrier-mediated process. If extensive ileal resection leads to bile salt loss which exceeds the compensatory increased liver synthesis, micellar concentration of bile acids necessary for fat absorption are inadequate. Steatorrhea, and lipid-soluble vitamin malabsorption are the consequence.

Additionally, with ileal resection, watery diarrhea may be exacerbated due to the effects of increased amounts of bile salts reaching the colon. Bacterial deconjugation and dehydroxylation of bile acids produces cathartic compounds. This situation is referred to as choleretic diarrhea (10). A high concentration of bile salts in the colon also causes secretion of sodium and water due to direct injury to the colonic epithelium and increased mucosal cyclic adenosine monophosphate levels (11). Enteral cholestryramine administration may be indicated in this situation, however, fat malabsorption may be exacerbated due to binding of bile acids. Thus, cholestryramine administration should generally be reserved for those children with SBS following extensive ileal resection, who have the small bowel in continuity with the colon, and have persistent problems with high volume stool losses.

Normally, most oxalate, commonly found in many foods, are rendered insoluble as calcium oxalate in the small bowel. When malabsorbed bile salts are present in the colon following distal small bowel resection, oxalates become more soluble and better absorbed. As a result, hyperoxaluria and renal lithiasis may occur in those children following extensive ileal resection who have an intact colon, and who consume a variety of foods. Hiperoxaluria is rarely seen in infants and children with SBS whose primary source of nutrition is a commercially prepared formula, because their oxalate intake is very low.

Children who have undergone partial or total colonic resection in addition to extensive small bowel resection, are more likely to develop fluid and electrolyte deficits. The colon has a large capacity to absorb water and sodium. The colon also absorbs and utilizes short-chain fatty acids as an energy source. Colonic resection generally has a greater negative effect in terms of fluid and electrolyte absorption than as a loss of a significant source of nutrient and energy absorption.

Although colonic resection or bypass may have negative effects in many instances, the presence of an intact colon may not always be favorable. When the colonic load of fatty acids is excessive, osmotic diarrhea may result. A child with a shortened small bowel who has lost the ileocecal valve, may occasionally have more severe complications associated with bacterial overgrowth when the small bowel is in continuity with the colon.

Preservation of the ileocecal valve may affect the prognosis. It performs functions which ultimately influence enteral feeding tolerance. The ileocecal valve regulates the flow of fluid and nutrients from the small bowel into the colon and the rate of small bowel transit. It also prevents migration of colonic bacterial flora into the small bowel.

Bacterial counts in the small bowel increase dramatically when the ileocecal valve is resected. Normal bacterial counts in the small bowel range from 103 proximally to 105 in the distal ileum . Bacterial overgrowth is usually defined as bacterial counts exceeding 105 in the small bowel. Other factors which may compound bacterial overgrowth in children with SBS include dysmotility and dilation of small bowel loops which favor stasis of bowel contents. These bacteria deconjugate bile salts, and the bile salt pool may become depleted with resulting fat and fat-soluble vitamin malabsorption. Bacteria also compete for nutrients, particularly vitamin B₁₂. Mucosal inflammation with small amounts of blood loss in the small and large bowel may also be caused by an overgrowth of bacteria.

The combined problems of small bowel bacterial overgrowth and carbohydrate malabsorption can lead to metabolic acidosis. Acidosis occurs when bacterial fermentation of unabsorbed carbohydrates produces short chain fatty acids including L-lactate an D-lactate (the latter which cannot be matabolized) which are then absorbed into the circulation.

Treatment should be aimed at decreasing the bacterial population in the small bowel with antibiotics, administration of low-carbohydrate formulas, and the addition of citrate or bicarbonate to the enteral or parenteral nutrition solutions. Metronidazole and timethoprim-sulfamethoxazole or non-absorbable aminoglycosides such as kanamycin and gentamicin, are often used in treatment alone or in intermittent regimens. The use of alternating courses of antibiotics may prevent the overgrowth of resistant organisms.

A fasting spot breath hydrogen test can be used as a screening tool for bacterial overgrowth. An excess of baseline hydrogen, prior to administration of carbohydrate, is suggestive of bacterial overgrowth. Confirmation of bacterial overgrowth may be obtained with cultures of duodenal fluid to determine the number and type of organisms. A history of abdominal symptoms, history of ileocecal valve resection or dysmotility, and the presence of metabolic acidosis are all highly suggestive of bacterial overgrowth which warrants treatment.

Motility Disturbances

Motility disturbances following small bowel resection occur frequently, and may compound problems associated with SBS including malabsorption and bacterial overgrowth . Proximal small bowel resection leads to a faster gastric emptying rate and the rate of emptying is direct1y correlated with the length of remaining jejunum (12). The ileocecal valve also serves as a mechanism to prolongs transit time of small bowel contents (13). When the distal small bowel and ileocecal valve are resected, loss of these slowing effects may lead to a dramatically increased rate of small bowel transit. The length of remaining colon also affects intestinal transit. The condition of the remaining bowel may have a more significant impact on motility and absorption than the total length and location of bowel resected. Stasis due to fibrosis, surgical narrowing or poor perfusion can be as detrimental to enteral feeding success as is fast transit.

Gastric acid hypersecretion is a common problem associated with SBS. The severity of gastric acid hypersecretion is proportional to the amount of small bowel resected (14). Removal of an inhibitor of gastrin secretion with small bowel resection has been attributed as the cause. Gastrin levels may remain elevated for years (15). Gastric acid hypersecretion may contribute to malabsorption by inactivation of pancreatic enzymes, interference with micellar formation and fat lipolysis, and peptic inflammation of the stomach and proximal small bowel. Treatment with H2 - receptor antagonist drugs, such as ranitidine or famotidine, or more potent proton pump inhibitors, such as omeprazole may be indicated in a child with upper gastrointestinal symptoms or biopsy proven endoscopic findings of peptic disease.

Following extensive small bowel resection, a marked adaptation response occurs in the residual bowel. This response is the primary source of increased absorptive surface area in the small bowel, and the primary reason many infants and children are able to be eventually weaned from parenteral nutrition support to full enteral feedings. These compensatory changes begin within days of bowel resection and last for many months. The most striking feature of adaptation is hyperplasia of the villus cells. The villus height increases with an increase in the number of epithelial cells and elongation of the crypts. The degree of hyperplasia appears to be direct1y proportional to the amount of small bowel resected. The adaptation potential is greater in the ileum following a proximal resection than in the jejunum following a distal small bowel resection (9).

Several factors appear to be trophic for small bowel adaptation, and the most important stimulus for adaptation is enteral feeding. The presence of nutrients in the lumen of the small bowel are essential for maintenance and restoration of mucosal mass. Mucosal atrophy in humans and animals occurs following starvation, and occurs even when adequate parenteral nutrition is provided as the exclusive source of energy. The height of microvilli dicreases and disaccharidase activity declines following 21 days of parenteral nutrition compared with preparenteral nutrition values in adults (16). The resumption of oral feeding leads to restoration of enzyme levels.

Nutrients in the small bowel lumen stimulate mucosal adaptation through several mechanisms including: 1) direct contac and absorption of nutrients by enterocytes, 2) stimulation of pancreatic and biliary secretions, and 3) stimulation of trophic hormones and growth factors in the bowel and elsewhere. The jejunum normally has greater absorptive surface area with longer villi likely due to vast exposure to nutrients compared to the ileum. Following proximal small bowel resection, increased exposure to nutrients leads to villus hyperplasia in the ileum. The residual jejunum may adapt less well than the residual ileum following bowel resection, because the absorptive capacity of the jejunum may already be near its highest level. The ileum generally has a greater capacity for change and adaptation as direct exposure to nutrients increases.

 Studies regarding the capacity of specific nutrients to stimulate adaptation have been conducted primarily in animals. Long-chain triglycerides fed to rats after bowel resection stimulate adaptation to a greater degree than proteins and carbohydrates (17). Medium-chain triclycerides have not been shown to have the same effect as long-chain triglycerides, and free fatty acids have been found to be superior to long-chain triglycerides as a stimulus for bowel adaptation (18).

Short-chain fatty acids, primarily acetate, propionate and butyrate are used for energy by the colon. These short--chain fatty acids are the product of bacterial fermentation of unabsorbed carbohydrates and fiber and are particularly trophic for the colonocyte. There is evidence that the administration of short-chain fatty acids into the colon stimulates mucosal growth in the colon and small bowel (19-20). Additionally, colonic absorption of short-chain fatty acids can supply 5-10% of daily energy requirements (21).

Although it has been suggested that complex diets stimulate small bowel adaptation, there is no clear indication that whole protein is superior to protein hydrolysates (22). Numerous studies in recent years have focused on the role of glutamine as a preferred fuel for the enterocyte and to promote the bowel adaptation response. These studies, conducted in animals, include both parenteral and enteral infusions of glutamine. Oral diets supplemented with glutamine fed to rats following small bowel resection have been shown to result in greater villus hyperplasia compared to isonitrogenous diets (23). Parenteral nutrition solutions containing glutamine, administered as the sole source of nutrition, have been associated with preservation of small bowel mucosa in rats (24,25). No commercially prepared parenteral amino acid solutions contain glutamine due to stability issues , but several enteral formulas containing glutamine are now available.

Various sugars have also been shown to promote small bowel adaptation. Sucrose, maltose and lactose infusions into the gastrointestinal tract of rats stimulate greater adaptation than monosaccharides (26) . The process of hydrolysis of disaccharides may contribute to the adaptation response.

Finally, numerous hormones have been found to have trophic effects on the small bowel. Gastrin appears to have a trophic effect on the proximal small bowel (27). Cholecystokinin also appears to have an effect secundary to hormonal stimulation of pancreatic and biliary secretions (28). Enteroglucagon is elevated in the serum of patients who have undergone intestinal resection or bypass (29). In animal studies, plasma enteroglucagon levels are increased in proportion to the amount of bowel resected and the crypt cell production rate in the residual bowel (30,3l). Prostaglandin analogues, epidermal growth factor and growth hormone have been found to be trophic in animals (32,33), adequate human studies are still lacking.

Recent studies have been conducted to assess the effects of co-administration of growth hormone, supplemental glutamine, and a modified fiber-containing diet on nutrient absorption following extensive bowel resection. The combined administration of these agents resulted increased sodium and nutrient absorption in adult subjects with SBS (34). There is limited experience with the use of this combination of therapeutic agents in children.

The evidence is strong that feeding into the small bowel is trophic, despite the fact that the exact mechanisms and relationship with enteric hormones and growth factors remains unknown. The potential enhancement of the intestinal adaptation response with administration of specific nutrients alone, or in combination with humoral or growth factors is the subject of ongoing research with promising hopes for further improvement in patient care for children.

Infectious complications associated with SBS may be related to the provision of long-term parenteral nutrition. In addition to small bowel bacterial overgrowth, central intravenous catheter infections pose a potentially serious risk. These infections can occur due to contamination of the parenteral nutrition solutions, administration sets, the catheter itself, or via the catheter insertion site. The intestine may also be a source. Bowel bacterial overgrowth and bowel atrophy, which may foster increased intestinal permeability of bacteria, may contribute to bacterial translocation and increase the risk of catheter infections. Repeated infections may increase metabolic demands and place greater pressure on adequate total delivery of enteral and parenteral energy.

Central venous access may become limited in children with SBS when multiple central lines lead to extensive venous thrombosis. Preservation of catheters in these circumstances becomes a priority. Catheter tip clots have been implicated as a contributing factor in central venous catheter infections. Theoretically, if bacteria or yeast are sheltered in a thrombus, then lysis of the clot might aid in treatment. Persistent bacteremia despite antibiotic therapy which was subsequently cured following catheter treatment with urokinase has been reported (35). The concomitant use of antibiotics and urokinase resultated in clearence of the organism from the blood in all 59 episodes of sepsis, with only 3 catheters requiring removal due to recurrent sepsis within 2 months, in a group of pediatric hematology-oncology patients (36). Approximately 20% of central intravenous catheters are removed due to infection according to a study of catheters and causes for removal in children (37). In our experience, approximately 90% of central intravenous catheter bacterial infections can be cleared with antibiotics alone, without line removal. More studies are needed to in order to determine if the incidence of catheter infection is decreased with the prophylactic use of urokinase.

Cholestasis is a frequent complication in children who require long-term parenteral nutrition. Although the mechanisms contributing to this problem are not fully understood, there is strong evidence that both prolonged parenteral nutrition and a lack of enteral feeding play independent, and significant roles. Small bowel bacterial overgrowth, carnitine deficiency, prematurity, infections, and multiple surgical procedures have also been associated with parenteral nutrition-associated cholestasis (PNAC).

Each of the nutritional components of parenteral nutrition solutions have been implicated in the development of PNAC. Multiple studies of PNAC have led to theories that increased dextrose intake may result in increased hepatic glycogen or fat deposition as the cause (38,39). In general, it is accepted that overzealous delivery of parenteral energy in the form of glucose can lead to cholestasis, probably due to the development of hepatic steatosis. In a rabbit model, however, parenteral glucose infusion did not show an effect on PNAC (40).

Parenteral lipids have also been suggested as an etiologic factor in the development of PNAC, however, currently available lipid emulsions do not contain cottonseed oil (suggested culprit), and have not been found to be associated with PNAC (41-43). Findings from several studies indicate that amino acids may be a significant contributor in the pathogenesis of PNAC (40,44). In a rat model, Moss et al., suggested that toxicity appears to be caused by free amino acids in parenteral nutrition solutions since intact protein administration did not result in cholestasis (45). A decreased incidence of cholestasis in newborns receiving enteral protein instead of intravenous amino acids has also been noted (46). We have recently reported our experience with resolution of PNAC in 5 children with severe malabsorption by replacing protein delivery from the parenteral to enteral route while maintaining adequate visceral protein status and growth (47). An obstacle to advancement of enteral feedings in patients with SBS is usually marked intolerance due to malabsorption of carbohydrate. Advancing enteral protein selectively did not lead to significant intolerance, and a significant amount of parenteral energy and fluid delivery was maintained via the parenteral route.

Lack of enteral feedings has frequently been cited as a significant risk factor for the development of PNAC. Dimínished hormonal simulation of hepatobiliary development and bile flow (48) and an increase in toxic bile acid formation (49) have been suggested as mechanisms contributing to cholestasis in the absence of enteral feeding. The absence of enteral feeding causes decrease in release of cholecystokinin, which is a stimulus for emptying of the gallbladder. Atrophy of the bowe1 occurs in the absence of enteral feeding, with subsequent dysmotility and stasis. With impaired intestinal motility, bile acids are metabolized to a greater degree with production of toxic end products of bacterial reduction such a lithocholic acid.

Intestinal bacterial overgrowth, particularly anaerobic organisms, have been associated with the pathogenesis of cholestasis in patients with SBS. Treatment with metronidazole at the onset of parenteral nutrition administration in patients with Crohn's disease (50) and jejunoileal bypass surgery (51) prevented liver enzyme abnormalities and hepatic steatosis characteristically seen in similar patients not treated with enteral antibiotics. Although the mechanism by which intestinal bacterial overgrowth causes hepatic dysfunction is unknown, production of hepatotoxic substances, such as bacterial cell wall toxins (52) and bile acids (53) have been proposed.

Case reports have linked hyperbilirubinemia with carnitene deficiency in patients receiving long-term parenteral nutrition, with resolution following addition of parenteral carnitene (54--55). Although phenobarbital has long been considered as the primary pharmacologic agent in treating PNAC, ursodeoxycholic acid has been more effective in decreasing elevated bilirubin levels (56). Although these therapies may contribute to improvement in cholestasis, in general, it is widely accepted that early institution of enteral feedings and weaning of parenteral nutrition are the most important interventions to reduce cholestatic liver injury.

Following the initial surgical interventions, management of nutritional therapy should become the focus of care for these children. Maintaining optimal nutritional status and growth, with a combination of parenteral and enteral nutrition support, should be a priority for infants and children to enhance general well-being and to prevent complications secondary to chronic undernutrition. Ma1nutrition should not be considered an inevitable complication of SBS. Enteral feeding also serves as a primary therapy in promoting bowel adaptation which is essential for long-term survival without dependence on parenteral nutrition.

The goals of parenteral nutrition therapy include maintenance of fluid and electrolyte balance and support of rapid growth during infancy and childhood while bowel adaptation occurs. Placement of a central intravenous catheter is often indicated for adequate delivery of long-term parenteral nutrition. Parenteral nutrition may be initiated very early; adjustments in total caloric delivery via parenteral nutrition should be adjusted based on the child's growth. Standard commercial parenteral trace element and pediatric multivitamin solutions are adequate to meet the needs of most infants and children requiring long--term parenteral nutrition, if administered at least 5 times per week, even those with SBS and large stool losses (57).

Fluid and electrolyte composition often needs to be individualized. Many infants and children require a greater than maintenance volume of fluids and electrolytes due to excessive stool losses. Parenteral solution electrolyte composition should be tailored to meet the individual needs of the child, calculating maintenance requirements plus ongoing losses. If fluid and electrolyte balance is difficult to maintain with one parenteral nutrition solution for several days, an electrolyte solution may be needed to replace stool losses on a volume basis every 4-12hours. Stool electrolyte composition can be determined to aid in the choice of parenteral electrolyte solution for replacement of losses.

During the early post-operative period, serum electrolytes, glucose, blood urea nitrogen, creatinine, calcium, phosphorus, triglycerides, bilirubin levels, AST, ALT, alkaine phosphatase and albumin should be monitored daily. Once relative stability with serum chemistry values is achieved, laboratory monitoring can be made less frequently. Some long-term patients may require monitoring every 1-6 weeks.

The first major accomplishment for children with SBS is achieved when parenteral nutrition support is no longer required, thus the goal of parenteral nutrition weaning during advancement of enteral feeding should remain a high priority. When only a small part (less than 25%) of energy is delivered parenterally, weaning can be accomplished by decreasing days of parenteral nutrition administration, rather than delivering smaller volumes daily.

Enteral feeding should begin as soon as possible following small bowel resection, once fluid and electrolyte balance is achieved and gastrointestinal motility has returned. Limited age-appropriate oral feedings (low fructose and lactose) should be encouraged throughout enteral feeding advancement, and increased once hours off continuous feeding is possible. The early introduction of small amounts of oral fluids and solids may prevent oral hypersensitivity and food aversion later when the bowel can tolerate more complex foods.

Assessment of a child's enteral tolerance should included general clinical status, gastrointestinal symptoms and growth. Measurements of clinical status include fluid and electrolyte balance, acid/base balance, hematologic status, visceral protein status, vitamin and mineral status and liver function. Assessment of gastrointestinal symptoms includes vomiting gastroesophageal reflux, abdominal distention, abdominal discomfort, stool volume and stool frequency. The severity of gastrointestinal symptoms should be judged on whether they compromise clinical status and the level of tolerance for the child and caregivers. Table I outlines general principles of dietary management of GI symptoms.

During the advancement of enteral feeding, parenteral nutrition should be continued for the balance of the child 's caloric needs, based on his or her rate of growth and specific nutrient status. The goal should be to maintain normal growth while promoting bowel adaptation.

TABLA I DIETARY MANAGEMENT OF GI SYMPTOMS
Vomitig/gastroesophageal reflux	Feeding volumen or concentration rate of administration, extend hours
Abdominal distension/increased stoll volume	carbohydrate, fat in necesary rate of administration, extend hour feeding volume or concentration
Increased stoll frecuency/watery Stool/diaper	feeding volume or concentration carbohytrate Add dietary fiber
Persistence any of the above	consider an amino/acid bases formula

 

Specific Feeding Recommendations

Malabsorption of protein, carbohydrate and fat all occur with SBS. Initial enteral feedings should be provided as continuos infusion via nasogastric or gastrostomy tube. Improved enteral balance, in terms of fat, nitrogen and micronutrient absorption has been documented in 11 infants with protracted diarrhea and SBS, with continuous tube feeding compared to intermittent oral feeding (58). Significant increases in body weight during continuous feeding compared to intermittent feeding was also noted. The greatest number of hours per day possible should be utilized for continuous infusion of formula to maximize absorption.

A formula containing hydrolyzed protein should be used, concentrated to 10-20 calories/ounce. Protein hydrolysates have the advantage of being more readily absorbed than whole protein (59). Despite some evidence that complex diets may be more trophic than elemental diets, there is no clear indication that an intact protein is better than a protein hydrolysate inenhancing mucosal hyperplasia (22). A significant amount of protein is absorbed in the small bowel in the form of di-and tri-peptides, so use of formulas containing only amino acids often is unnecessary. There may be an indication, in selected children with SBS , for the administration of amino acids as the sole source of enteral protein when evidence of allergic colitis or gastroenteritis is present (60). We have found that several infants with eosinophilic inflammation of the stomach and small bowel and peripheral eosinophilia have benefitted from the use of an amino acid formula . Most of these infants demonstrated persistent vomiting with standard protein hydrolysate formulas. Among the mechanisms contributing to allergic gastroenteropathy in children with SBS may be an increased permeability of the small bowel to antigenic molecules for a period of time following the initial insult.

The role of carbohydrate in dietary management of SBS requires much attention. Carbohydrate in the form of glucose polymers , is frequently to increased caloric density of formulas and intake. Severe malabsorption of carbohydrate, however, contributes to osmotic diarrhea and metabolic acidosis through bacterial fermentation and increased absorption of short chain fatty acids (SCFA) , including D--lactate. In infants and children, the amount and rate of SCFA produced can overwhelm the capacity to metabolize them and lead to severe acidosis following increases in carbohydrate in the diet. In this situation, carbohydrate often needs to be restricted, hindering the advancement of enteral feedings. The presence of reducing substances in the stool and stool pH less than 5.5 provides evidence of carbohydrate malabsorption. A low stool pH and metabolic acidosis are indicative of carbohydrate malabsorption and intestinal fermentation.

Complex starches should be avoided initially because they require considerable digestion before absorption can occur. Lactose should also be avoided because lactase activity in the injured or shortened bowel is usually significantly decreased. Glucose does not require hidrolysis for absorption, and therefore, may be more readily absorbed. Unfortunately, formulas containing only glucose may be hyperosmolar, which can impair fluid absorption and worsen diarrhea. Some infants and children with SBS cannot tolerate commercial formulas which contain glucose and glucose polymers as 40-55% of total calories. The administration of an enteral formula with a combination of glucose or sucrose with glucose polymers is most likely the best carbohydrate source for infants and children with SBS. If carbohydrate malabsorption is severe, a commercial formula with little or no carbohydrate is recommended. Carbohydrate, in the form of dextrose, can be added and titrated as absorption improves.

Traditionally, dietary recommendations for children and adults with SBS have included low-fat, low-fiber diets (61-64). These dietary recommendations were based on the fact that lowerfat diets have been associated with decreased steatorrhea and decreased stool water and electrolyte losses (63,65), and that high fiber diets have been associated with increased ileostomy output (66). These recommendations have been associated with improved symptoms but not with improved nutritional status or successful advancement of enteral feeding.

Recently, researchers and clinicians have challenged this premise and shown that high-fat diets resulted in improved weight gain without increased fat malabsorption or stool volume in patients with protracted diarrhea on infancy and cystic fibrosis (67,68). Additionally, there are reports of little benefit from fat restriction in adults with SBS and high jejunostomies (69-7l). We have reported our experience with low-carbohydrate, high-fat diets (up to 65% of enteral calories as fat) with medium-chain triglycerides to successfully advance enteral feedings in 13 infants and young children with SBS (72). Even when total stool fat increases with high-fat enteral feedings, if the child absorbs a fraction of the incresed fat and more net calories, then high-fat feedings can prove beneficial. There are no reports, to date, of lipid abnormalities resulting from high-fat enteral feedings in children with SBS and chronic malabsorption. Laboratory monitoring is needed to prevent potential complications such as hyperlipidemia, hypocalcemia, ketosis and hypoglycemia.

The use of medium-chain tryglicerides in the dietary management of SBS was suggested as early as 1966 (73). Medium-chain triglycerides are more readily absorbed than long-chain triglycerides in the abscence of sufficient bile acids, as medium-chain triglycerides may pass direct1y into the portal circulation. The use of medium-chain triglycerides improves fat and total energy absorption. Current recommendations for enteral feeding of children with SBS include high-fat diets with medium-chain triglycerides as the primary fat source (74-76). Some long-chain triglycerides (approximately 10% of total calories) are needed in order to prevent essential fatty acid deficiency. They also appear to be more trophic in stimulating mucosal hyperplasia, and free fatty acids may be even more advantageous in this regard (18). Enteral modules of long-chain triglycerides may be added to the formula to meet this goal.

The addition of fiber to enteral feeding may be beneficial. Soy fiber, added at a dose of 10 to 15 gm/L, may help regulate transit time and improve stool consistency in children with SBS. This may be very important for the infant or child with severe perineal skin inflammation due to passage of frequent, watery stools. The addition of fiber may result in worsening acidosis, however, presumably from increased bacterial fermentation in the bowel, if bacterial overgrowth is not controlled.

Advancements in enteral feeding should be made at regular intervals, as tolerated, with increased volume or concentration of formula. If carbohydrate malabsorption is documented, a low carbohydrate formula may be used with gradual addition of dextrose or glucose polymers. Commercial formulas with glucose polymers, protein hydrolysates and MCT oil may be increased in caloric density above 20 cal/oz by adding a protein hydrolysate module or additional MCT oil rather than concentrating the formula which increases carbohydrate intake. In our experience, the use of high-fat, low-carbohydrate diets has accelerated the transition from parenteral nutrition to complete enteral nutrition in children with SBS (72). Parenteral calories, fluid, electrolyte and micronutrient (vitamins and minerals) support: should be continued to maintain appropriate growth and nutrient status. Table II includes guidelines for enteral feeding advancement.

Once complete enteral nutrition is achieved, compression of continuous feedings can be attempted, with increased hourly infusion rates with less hours of feedings during the day. Oral feedings (low fructose and lactose) can be encouraged and advanced once «hours off» , continuous feedings are possible. Once full enteral feedings are achieved and parenteral nutrition has been discontinued, specific nutrient deficiencies are much more likely to occur. Poor absorption of fat-soluble vitamins, minerals and trace metals are common. It is during this phase of nutritional intervention that frequent micronutrient lab monitoring is warranted.

Supplemental enteral multivitamin and mineral products should be administered. Severe deficiencies may be corrected with additional individual micronutrients administered enterally or parenterally. Numerous medications often will also be malabsorbed, necessitating administration by the parenteral route. For example, oral antibiotics prescribed for cornmon pediatric infections may be poorly absorbed by children with SBS with unpredictable therapeutic effects.

Although practical difficulties with enteral feedings are common in children with SBS, there are many strategies which can enhance delivery of nutrition support and improve the child's and family's quality of life. With creative and persistent efforts to manage parenteral and enteral nutrition, malnutrition should never be considered an inevitable consequence of SBS.

 

Use of Oral Rehydration Solutions

Oral rehydration solutions should be routinely used to replace fluid and electrolyte losses, particularly during acute illness, when enteral feedings are being advanced and when parenteral nutrition has been discontinued. Often a child's hydration and electrolyte balance may be maintained on enteral fluids alone for a period of time while awaiting placement of a new central intravenous catheter with the liberal use of oral rehydration solutions provided by mouth or by feeding tube. Also, oral rehydration solutions may be incorporated into the formula on a daily basis to help maintain electrolytes within normal limits in children on complete enteral nutrition with high sodium and potassium requirements. The use of oral rehydration solutions with formulas takes advantage of the sodium-glucose cotransporter present in the intestinal epithelium and stimulate active sodium absorption and subsequent water absorption by solvent drag (77).

TABLA II Advancement of enteral feeds in SBS

1. start with protein hydrolysate formula containing MCT-10 cal/oz as continuous tube feeding for as many hours per day as possible, at a modest rate

2. Advances concentration to 20 cal/oz and advance rate of administration as tolerated

3. If carbohydrate malabsorption is severe, change to a low-carbohydrate formula and titrate added glucose as tolerated

4. If unable to add carbohydrate or concentrate formula >20 cal/oz, advance with added with MCT oil or protein hydrolysate module.

5. Advance formula concentration or rate of administration -biweekly as tolerated

6. Continue parenteral kcals, protein, fluid and micronutrients as needed to maintain normal growth and nutritional status.

7. Monitor for fluid, electrolyte and acid/base imbalences, hypoglycemia, ketosis, hypocalcemia, essential fatty acid diciency and hyperlidemia

8. Throughout: encourage oral feeding of small amounts of varied food taste and texture. Avoid large amounts of highly osmolar or high carbohydrate feeds, especially lactose/fructose.

 

SURGICAL MANAGEMENT

Although nutritional and medical therapies are the primary forms of treatment for SBS, additional surgery may be indicated. If severe dilatation of the small bowel occurs, with persistent feeding intolerance, bacterial overgrowth and malabsorption due to stasis and dysmotility, an intestinal tapering procedure may be beneficial. Strictures or adhesions which cause partial obstruction with severe dilatation and stasis, may require surgery in order to allow independence from parenteral nutrition. The risk/benefit ratio must be carefully reviewed, as further bowel resection or abdominal surgery may lead to new adhesions and strictures or loss of mucosal surface area. Many other surgical interventions, including the creation of intestinal valves, antiperistaltic segments, recirculating loops, and intestinal lengthening procedures, have been attempted in order to delay intestinal transit time or increase absorptive surface area. Delaying intestinal transit may actually be detrimental in some cases, by worsening stasis and bacterial overgrowth. None of these surgical procedures is yet sufficiently safe and successful to be used routinely (78).

Despite numerous potential problems, recent success with intestinal transplantation has expanded the treatment options for children with SBS. Preliminary results indicate that combined liver and small bowel transplants and isolated intestinal transplantation may be viable options for some patients with severe intestinal and liver disease (79-81). At this time, candidates for isolated small bowel transplantation or combined liver and small bowel transplantation include those with a permanent dependence on parenteral nutrition or severe complications related to long-term parenteral nutrition.

 

HOME CARE

When long-term nutrition support is anticipated, preparation of the family for home care should begin as soon as possible. This is usually feasible as soon as fluid and electrolyte balance and nutritional status is adequate and relatively stable. Home care is beneficial to prevent lengthy hospitalization and associated problems such as increased rates of infection, developmental delay and family stress. Most infants and children with SBS can be successfully care for at home with parenteral and enteral nutrition.

The caregivers must be thorough1y educated about nutritional therapy administration and parenteral and enteral access care, and they should be provided with adequate support services. Most of these children and families will benefit from home nursing services to assist with and supervise therapy. Portable parenteral and enteral feeding pumps are now widely available, which enable the child and family to maintain a more active life-style. Parenteral nutrition should be cycIed, if possible, to allow some time off the intravenous infusion equipment each day. Health care providers should advocate for necessary supplies and services for home care. Close follow-up care by an interdisciplinary nutritional support team is essential. Provision of long-term nutrition support at home has been one of the most dramatic changes in the past decade in the management of the child with SBS.

 

SUMMARY

Successful management of complex nutrition support has provided the opportunity for long-term survival and a desirable quality of life for many children with SBS. Early and aggressive enteral feeding is the primary stimulus for intestinal adaptation, which is the key to ultimate independence from parenteral nutrition and prevention of associated complications. Ongoing research regarding the composition and delivery of nutrition should enhance the care of children with SBS, prevent complications and expedite recovery. Additional experience with non-medical therapies, including intestinal transplantation, will expand the treatment options for those children with severe complications precluding continued parenteral nutrition.

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