Current Strategies in Surgical Nutrition

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Management of the Short -bowel Syndrome

Stanley]. Dudrick, MD,* RifatLatifi, MD,t and David E. Fasnacht, MDt.

The short-bowel syndrome is not a clinical entity precisely defined by a specific length of residual functioning small intestine, but rather an aggregation of clinical signs and symptoms characterized primarily by intractable diarrhea, steatorrhea, weight loss, dehydration, malnutrition, and malabsorption of fats, vitamins, and other nutrients. Secondary or more specific subsequent consequences of the syndrome include hypovolemia, hypoalbuminemia, hypokalemia, hypocalcemia, hypomagnesemia, hypozincemia, hypocupricemia, fatty acid and vitamin deficiencies, anemias, hyperoxaluria, and metabolic acidosis. The actual presentation of the patient with short-bowel syndrome depends on several factors: (1) the extent of resection; (2) the site of resection; (3) the presence or absence of the ileocecal valve; (4) the residual function of the remaining small bowel, stomach, pancreas, biliary tree, and colon; (5) the adaptative capacity of the intestinal remnant; (6) the primary disease that precipitated the loss of the small bowel; and (7) the amount and activity of the residual disease in the intestinal remnant. 3 • 21. 27. 39. 96 The minimum length of small bowel sufficient for adequate absorption is controversial because of the variable absorptive capacity of the remnant, the wide variation in the length of the normal small intestine, and the difficulty in obtaining reproducible measurements of the length of the bowel remaining after massive resection. Depending on its state of contraction or relaxation, intraoperative estimates of the length of the normal intact small intestine in the adult range from 260 to 800 cm (approximately 8-26 feet).96 The mean length of normal small intestine during life is 350 cm (11-12 *Surgeon-in-Chief, Hermann Hospital; and Clinical Professor of Surgery, The University of Texas Medical School at Houston, Houston, Texas tResearch Associate in Surgery, Hermann Hospital, Houston, Texas :j:Research Assistant, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania

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feet) and postmortem is 600 cm (20 feet). The great variability makes it difficult to determine the exact length of the remaining small bowel and makes it virtually impossible to estimate the percentage of the total length of the small bowel represented by the segment remaining after massive intestinal resection. Moreover, many surgeons not only measure the length of the resected small bowel, rather than measuring the length of the remaining intestinal segment, but then fail to describe accurately the nature and extent of the remaining small bowel in the patient's medical record for future reference. Furthermore, because inflamed bowel shortens after operation, the symptomatic outcome of massive small-bowel resection does not correlate well with the intraoperative estimated length of resection. 86 Because of its rather generous functional reserve capacity, resections of the small intestine usually do not result in significant problems with digestion and absorption. 26. 28 Indeed, resection of as much as 40% of the small intestine is usually well tolerated provided the duodenum, the distal half of the ileum, and the ileocecal valve are spared. 88 On the other hand, resection of 50% or more of the small intestine usually results in significant malabsorption initially but can be tolerated eventually without exceptional nutritional support. However, resection of 75% or more of the small intestine usually leaves the patient with 70 to 100 cm (2-3 feet) of intestine, resulting in a short-bowel syndrome that can significantly impair the ability of the patient to maintain normal nutrition and metabolism. This patient will likely require special nutritional care on a long-term or permanent basis, especially with the loss of the terminal ileum and the ileocecal valve. The severity of symptoms after massive small-bowel resection is related both to the extent of the resection and to the specific level of the resected small bowe1. 97 However, the minimal residual absorptive surface required to sustain life without permanent parenteral nutritional support appears to be different for each patient. 98• 10l The development of effective total parenteral nutrition (TPN) has revolutionized the treatment of the short-bowel syndrome by allowing maintenance of adequate nutrition until the remaining bowel can adapt maximally to oral feeding, thus reducing the morbidity and mortality rates significantly. 17. 24. 75, 80, 99,100 Long-term survival has now been achieved in a number of patients having an intact duodenum and 15 cm (6 inches) of residual jejunum, with or without the colon. 21 , 28 In addition to the entire duodenum, if approximately 60 cm (2 feet) of jejunum or ileum remains functional, survival has been the rule rather than the exception, Preservation of the ileocecal valve is of paramount importance during massive smallbowel resection and, by significantly increasing the intestinal transit time, appears to have the effect of increasing the absorptive capacity of the remaining small bowel to approximately twice that anticipated for the same length of small bowel without an intact ileocecal valve. Primarily as a result of mucosal hyperplasia and villous hypertrophy, absorption in the residual intestinal segments of patients with short-bowel syndrome can increase as much as fourfold. Therefore, in a patient with an intact ileocecal valve, the total absorptive capacity of the remaining bowel potentially can be increased as much as eightfold.

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CAUSE The most common clinical conditions that precipitate massive smallbowel resection are those which compromise the vascular supply of the small intestine. 32, 49, 83 These include venous thrombosis and arterial occlusion as a consequence of primary vascular disease, various coagulopathies, volvulus, malrotation of the gut, and internal or external herniation of the bowel with strangulation, Short-bowel syndrome can also occur congenitally as a result of massive atresia of the small intestine. Inflammatory bowel disease involving large segments of the small bowel, or recurrent exacerbations of inflammatory bowel disease over a long period of time, can eventually result in the short-bowel syndrome secondary to massive or multiple intestinal resections. Excision of retroperitoneal malignancies that involve the superior mesenteric vessels can mandate resection of most or all of the small bowel in order to accomplish palliation or cure. Major abdominal blunt or sharp trauma involving transection, disruption, or' avulsion of the mesenteric vasculature can result in ischemic necrosis of large segments of the small bowel, resulting in short-bowel syndrome. Postirradiation or postoperative complications such as extensive severe radiation enteritis, multiple bowel fistulas, and intestinal gangrene can also result in irreversible short-bowel syndrome. Iatrogenic short-bowel syndrome has been a method of weight reduction in morbidly obese patients and a means of plasma cholesterol reduction in patients with hypercholesterolemia. However, such jejunoileal bypasses are usually reversible surgically if indicated or desired.

PATHOPHYSIOLOGY

As stated earlier, the efficiency of absorption of fluid, electrolytes, and nutrients is dependent on the site and extent of the small-bowel resection. The intestinal phase of digestion occurs initially within the duodenum, where pancreatic enzymes and bile acids aid digestion of all nutrients and promote fat absorption. It is unusual for the duodenum to be resected together with extensive segments of the small bowel; however, total duodenectomy leads to malabsorption of calcium, folic acid, and iron. 3 Proteins, carbohydrates, and fats are absorbed virtually completely in the first 150 cm of the jejunum, so that only small quantities of these macronutrients ever reach the ileum. 12 The small intestine receives and processes about 8 L of fluid daily, including dietary ingestion and endogenous secretions. Normally, about 80% of the water transported is absorbed in the small bowel, leaving approximately 1.5 L of fluid to enter the colon. The colon usually absorbs 1 to 2 L of fluid, with a maximal absorptive capacity of approximately 6 L per day.20 Large proximal small-bowel resections, therefore, result in little diarrhea because the ileum and colon have a great capacity to reabsorb excess fluid and electrolytes. Conversely, extensive or total ileal resection produces a greater potential for malabsorption and diarrhea. Not only will this resection increase the volume of fluid reaching the colon, but, depend-

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ing on the length of the ileal resection, bile salt diarrhea (cholerrhea) or steatorrhea may ensue, with significant loss of fat-soluble vitamins. If the ileocecal valve has been resected, transit time may decrease, and bacterial colonization of the small bowel will eventually occur, aggravating both cholerrhea and steatorrhea. As the length of ileal and colonic resections is increased, essential absorptive surface area is lost, resulting in progressive dehydration, hypovolemia, and electrolyte disturbances. If the colon remains in continuity with the residual small bowel after massive resection, malabsorbed bile salts can be deconjugated by colonic bacteria, stimulating colonic secretion and aggravating diarrhea. With extensive ileal resection, an irreversible loss of bile salts occurs with or without the colon in continuity. Even though the excess losses stimulate hepatic synthesis of bile salts, a higher incidence of cholelithiasis occurs in these patients. Because the transit time in the ileum usually is slower than in the jejunum (and this remains so after massive intestinal resections), intestinal transit will be slowed, and fecal output will be lower as the length of residual ileum increases. After extensive small-bowel resections, intestinal lactase activity may be decreased, producing lactose intolerance. 72 The unhydrolyzed lactose can result in increased hyperosmolality in the intestinal lumen. Moreover, the fermentation of the lactose by bacteria in the colon can produce a large amount of lactic acid that can further aggravate osmotic diarrhea. 3 The water-soluble vitamins and minerals (vitamin B complex and C, Ca, Fe, Mg) are absorbed in the proximal small intestine, while Mg diffuses passively throughout the entire small bowel. 3 The ileum is the sole site for absorption of vitamin B12 and the bile salts. Jejunectomy with preservation of the ileum produces no permanent defects in the absorption of protein, carbohydrate, and electrolytes. 105 The ileum can compensate for most of the absorptive functions, but not for the secretion of jejunal enterohormones. Mter jejunal resections, decreased secretion of cholecystokinin and secretin decreases gallbladder contraction and pancreatic secretion. After jejunal resection, gastric hypersecretion is greater than after ileal resection. As a result of the loss of inhibitory hormones such as gastric inhibitory polypeptide and vasoactive intestinal polypeptide, secreted in the jejunum, gastrin levels rise, thus stimulating gastric hypersecretion. 81 Significant gastric hypersecretion can be documented within 24 hours postoperatively, and the mucosa distal to the stomach can be injured by the high gastric acid output. Subsequently, the high salt load secreted in the stomach, together with the inactivation of digestive enzymes by the low intraluminal pH, serves to compound the other causes of diarrhea already present in short-bowel syndrome. Normally, the colon functions as a major site of water and electrolyte absorption. As the ileal efRuent increases, the colon may increase its absorptive capacity threefold to fivefold. 64 Furthermore, the colon has a moderate capacity to absorb nutrients, and concomitant colon resections can affect the symptomatic and nutritional courses of patients with massive small-bowel resections. Malabsorbed carbohydrates that reach the colon are fermented by bacteria to yield short-chain fatty acids, principally acetate, butyrate, and propionate. 10, II Short-chain fatty acids can be absorbed by

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the colon in quantities up to 500 kcal per day and enter the portal circulation to become a fuel source for the body. 43, 65 Although retention of the colon is highly desirable, its presence is associated with potential complications. In addition to having choleretic diarrhea induced by the bile salts, patients with massive small-bowel resection and an intact colon have a tendency to form calcium oxalate renal stones. This results from the increased absorption of dietary oxalate, which is normally rendered insoluble by calcium in the intestinal lumen and, therefore, ordinarily is unabsorbable. However, in patients with short-bowel syndrome and steatorrhea, intraluminal intestinal calcium is bound preferentially to unabsorbed fatty acids, leading to decreased binding and increased colonic absorption of the oxalate. 97 Finally, preservation of the ileocecal valve during distal small-bowel resection is an important preventive determinant of the metabolic sequelae because the ileocecal valve ordinarily slows intestinal transit and prevents bacterial reflux from the colon into the small bowel. Nutrients that reach the intestinal lumen, especially vitamin B12, become substrates for bacterhll metabolism rather than being absorbed by the mucosa. 3 Furthermore, bacterial overgrowth in the small bowel in patients with short-bowel syndrome who are receiving TPN appears to increase the incidence of liver dysfunction. 16

METABOLIC MANAGEMENT In the metabolic and nutritional management of patients with the short-bowel syndrome, three therapeutic periods having distinctive characteristics can be identified (Table 1). During the first 2 months (the immediate postoperative period), the clinical picture and course are dominated by problems related to fluid and electrolyte balance, adjustment of organ blood flow patterns, especially the portal venous flow, and other effects of the major operative insult and its attendant specific and general complications. During the second period, from about 2 months to 2 years postoperatively (the bowel adaptation period), efforts are directed toward defining the maximum oral feeding tolerances for various substrates, encouraging and maximizing intestinal and bowel adaptation, and determining and formulating the most effective individualized feeding regimens. Usually, within 2 years, 90% to 95% of the bowel adaptation potential has been realized, and little further improvement in absorption and bowel adaptation can be antiCipated. The third period (long-term management) constitutes the period after 2 years, by which time nutritional and metabolic stability have occurred. At this point, the patient either has adapted maximally, so that nutritional and metabolic homeostasis can be achieved entirely with oral feeding, or is committed to receiving supplemental or complete nutritional support for the remaining lifespan, either by ambulatory home TPN, specialized enteral or oral feedings, or both. Immediate Postoperative Period During the immediate postoperative period, virtually all nutrients, including water, electrolytes, fats, proteins, carbohydrates, and all vitamins

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Table 1. Management of Short-bowel Syndrome 111MEDIATE POSTOPERATIVE PERIOD

BOWEL ADAPTATIO:,,[ PERIOD

LONG-TERM MANAGEMENT

(FIRST 2 MONTHS)

(FIRST 2 YEARS)

(AFTER 2 YEARS)

Fluid and electrolyte replacement Lactated Ringer's solution Dextrose 5% in water Human serum albumin K+, Ca2+, Mg2+ supplementation Strict intake and output monitoring Daily body weight Graduated metabolic monitoring Antacid therapy Camalox suspension Mylanta liquid Amphojel suspension Gelusilliquid (30-60 mL via nasogastric tube q 2 h clamp tube 20 min) or Carafate 1 g po q 6 h (clamp nasogastric tube 30 min) Antisecretory-antimotility therapy Cimetidine 300 mg IV q 6 h Ranitidine 150 mg IV q 12 h Famotidine 20 mg IV q 12 h Codeine 60 mg 1M q 4 h Loperamide 4-16 mg po daily Lomotil 20 mg po q 6 h Somatostatin 50-150 fLg SC q 6 h Cholestyramine 4 g po q 8 h TPN 1 L on second postop day Gradually increase dosage as tolerated Supplement fluids, electrolytes, and colloids as needed

Progression of oral diet Water, tea, broth Simple salt solutions Simple sugar solutions Complex salt/sugar solutions Dilute chemically defined diets High carbohydrate, high protein Near-normal, normal diet Enteral supplementation Coconut oil 30 mL po tid Saffiower oil 30 mL po tid Multiple vitamins 1 mL bid Iron 1 mL tid Ca gluconate 6-8 glday . Na bicarbonate &-12 glday

Apply previous principles as indicated individually Ambulatory home TPN Supplemental or total Continuous, cyclic or, intermittent Surgical maoagement Treat operative complications Drain abscesses Resect fistulas Lyse adhesions Reduce obstructions Restore bowel continuity Probable cholecystectomy

Parenteral supplementation Electrolytes Divalent cations Trace elements Albumin Packed erythrocytes Lipid emulsion Antisecretory-antimotility Famotidine 20 mg po q 12 h Pro-Banthine 15 mg po q 4-6 h

Omeprazole 20 mg po q day Deodorized tincture of opium 10-30 drops q 4 h Acetaminophen with codeine 30-60 mg q 4 h (Refer to column 1 for additional agents)

and trace elements, are absorbed from the gastrointestinal tract poorly or not at all. Fluid losses via the gastrOintestinal tract are greatest during the first few days after massive small-intestinal resection, and anal or ostomy effluent frequently reaches volumes in excess of 5 L per 24 hours. If lifethreatening dehydration, hypovolemia, hypotension, and electrolyte imbalances are to be minimized, vigorous fluid and electrolyte replacement therapy must be instituted promptly. Frequent vital signs, intake and output, and central venous pressure measurements, together with regular hematologic and biochemical indices, should be helpful in monitoring the patient during this period of rapid metabolic change and instability. All patients with short-bowel syndrome exhibit abnormalities in their liver profiles, and most of them experience at least transient hyperbilirubinemia. This is thought by some to be secondary to the translocation of microorganisms or their toxins through the ischemic or gangrenous intestinal mucosa into the portal vein and thence to the liver. Others attribute the jaundice to impaired blood flow to the liver through the portal vein by as much as 40% as a result of greatly diminished mesenteric venous return secondary to the massive small-bowel resection. Still others attribute the

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phenomenon to a combination of both factors or to other etiologies. Broadspectrum anaerobic and aerobic antibiotic therapy is instituted and maintained for several days to a week after massive intestinal resection. During this period, typical patient management efforts are directed toward four primary goals: fluid and electrolyte replacement, antisecretoryantimotility therapy, antacid therapy, and TPN. During the first 24 to 48 hours, replacement therapy usually consists of 5% dextrose in lactated Ringer's solution administered intravenously concomitantly with appropriate amounts of potassium chloride or acetate or both, calcium gluconate, magnesium sulfate, and fat- and water-soluble vitamins. Salt-poor human albumin (12.5-25 g) usually is added exogenously to each liter of crystalloid solution for the first 24 to 48 hours postoperatively in order to maintain normal plasma albumin concentration and normal plasma colloid oncotic pressure. In patients with severe diarrhea, zinc losses can increase to as much as 15 mg/day and will necessitate appropriate parenteral replacement. 104 Antacid therapy can reduce the tendency for peptic ulceration, which commonly occurs immediately after massive small-bowel resection. Antacids are instilled via a nasogastric tube every 2 hours in doses of 30 to 60 mL, and the tube is clamped for 20 minutes before reapplying suction and repeating the sequence. Alternatively, sucralfate can be given by mouth or via the nasogastric tube in a dose of 1 g every 6 hours, clamping the tube for 30 minutes after each dose. To counteract the hypergastrinemia and associated gastric hypersecretion that follows massive small-bowel resection in the majority of patients, an H2 blocker is prescribed. 18 The intravenous (IV) infusion of 300 to 600 mg of cimetidine (Tagamet) every 6 hours can have a profound effect in reducing gastric acid and intestinal fluid production. Alternatively, ranitidine (Zantac) 150 mg can be given IV every 12 hours, or famotidine (Pepcid) 20 mg can be given IV every 12 hours. In some patients, somatostatin analogue (Sandostatin) has reduced fecal losses when given in a dosage of 50 to 150 f.lg IV or subcutaneously (sc) every 6 hours. 48 ,60 If diarrhea remains persistent despite these measures, an opiate can be used. Preferably, codeine is given in doses of 60 mg intramuscularly (1M) every 4 hours. Improvement in fluid and electrolyte management can also be achieved in selected patients who have stomal access to a distal defunctionalized bowel loop by reinfusing the chyme from the proximal ostomy into the distal fistula. 50 Later in the postoperative period, when the patient is tolerating liquids by mouth, oral antimotility therapy can be achieved by giving loperamide (Imodium) 4 to 16 mg in divided doses daily, cholestyramine (Questran Light) 5 g every 4 to 8 hours, or diphenoxylate (Lomotil) 20 mg every 6 hours. Codeine-acetaminophen (Tylenol 3) administered orally every 4 hours in doses of 30 or 60 mg, or deodorized tincture of opium 10 to 30 drops every 4 hours orally, can be used to impede bowel motility. The only form in which oral codeine is available currently is in combination with acetaminophen, which does not seem to compromise its effectiveness. The major advantage of giving the tincture is that the patient's bowel hypermotility and diarrhea can be titrated to tolerable levels by adjusting the dosage up or down a few drops at a time.

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By the second or third postoperative day, the patient's cardiovascular and pulmonary status usually has stabilized sufficiently so that TPN can be instituted. The average adult patient usually can tolerate an initial ration of 2 L of TPN solution administered by central vein during the first 24 hours of infusion (Table 2). By titrating against the indices of plasma glucose and glycosuria, the daily nutrient intake can be increased gradually to the desired level or to tolerance. In a patient with diabetes mellitus, or in one who is glucose intolerant, crystalline human insulin can be added to the TPN solution in doses up to 50 ulL (1000 kcal). After an operation of the magnitude of massive small-bowel resection, most patients require 3000 to 4000 mL ofTPN solution (3000 to 4000 kcal) per day to maintain nutritional homeostasis. Supplemental fluid and electrolyte infusions may be necessary for several days or weeks to balance the excessive gastrointestinal tract losses as diarrhea. Table 2. Adult Total Parenteral Nutrition Solution Base solution 40%-50% dextrose in water 8.5%-15% crystalline amino acids Additives to each liter Sodium chloride, acetate, or lactate Potassium chloride Potassium acid phosphate (10-20 mmol phosphorus) Magnesium sulfate Additives to anyone liter daily Calcium gluconate 10% Zinc sulfate Copper sulfate Iron-dextran Chromium chloride Manganese chloride Selenium (sodium selenate) Multivitamin infusion 3300 IU A 200 IU D lOIU E 100 mg Ascorbic acid 400 f.Lg Folic acid 40 mg Niacin 3.6 mg Riboflavin 3.0 mg Thiamine 4.0 mg B6 (pyridoxine) 5.0 f.Lg B12 (cyanocobalamin) 15 mg Pantothenic acid 60 f.Lg Biotin Additive to anyone liter twice weekly Vitamin K IV fat emulsion 10% or 20% 200-500 mL two to seven times weekly Carbohydrate energy Protein energy Fat energy Nitrogen Amino acids

500 mL 500 mL 40-50 20-30 15--30 15-18

mEq mEq mEq mEq

4.6-9.2 mEq 5-10 mEq 1-2 mEq 0.1 mL 10-20 f.Lg 0.5 mg 60 f.Lg 10 mL

10 mg 20-100 g

850 kcaVL 150 kcaVL 1000-2000 kcaVL 6.5-8.0 giL 40-50 giL

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The patient is started on a simple clear liquid diet as soon as the postoperative condition is stabilized, and fecal output is controlled with antidiarrheal medications. It may take several days to several weeks before the patient will be able to relinquish TPN support in favor of oral or enteral feedings. It is important to maintain adequate nutritional status with TPN for as long as the patient requires support. The TPN ration is reduced gradually in a reciprocal manner as oral intake and intestinal absorption of required nutrients are increased. The patient is advanced slowly and gradually to a low-lactose, low-fat, high-protein, high-carbohydrate diet according to individual tolerances to the nutrient substrates and to the water volume and osmolality of the dietary regimen. 61 Bowel Adaptation Period During the period of bowel adaptation, the patient is allowed to consume increasing quantities of water, simple salt solutions, and simple carbohydrate solutions. Various fruit and other flavorings can be added to' 5% dextrose in lactated Ringer's solution as a relatively inexpensive and practical start-up oral solution. Gradually, dilute solutions of chemically defined diets that contain simple amino acids and short-chain peptides are offered as tolerated in increasing volumes and concentrations as bowel adaptation progresses. Feeding should be progressive toward a normal or near-normal diet consisting of high carbohydrate, high protein, and modest fat and consisting of foods preferred by the patient as the next step in nutritional rehabilitation. Alternatively, the major macronutrients can be provided as required in commercially prepared modular feedings tailored to the needs of the individual patient until ordinary food is well tolerated. All essential vitamins, trace elements, and essential fatty acids and minerals are initially supplied in the patient's balanced intravenous nutrient ration. Subsequently, the oral diet may be supplemented most economically by short- and medium-chain triglycerides in the form of coconut oil, 30 mL two or three times daily; essential fatty acids as saffiower oil, 30 mL two or three times daily; multiple fat- and water-soluble vitamins in pediatric liquid form, 1 mL twice daily; vitamin B12, 1 mg 1M every 2 to 4 weeks; folic acid, 15 mg 1M weekly; and vitamin K, 10 mg 1M weekly. Some patients may require supplemental iron, which may be administered initially by deep 1M injection as iron-dextran according to the recommended dosage schedule, or as an IV infusion after testing the patient for sensitivity. Alternatively, Fer-In-Sol 1 mL can be given one to three times daily. The strong tendency for patients with short-bowel syndrome to develop metabolic acidosis often mandates the use of sodium bicarbonate powder, tablets, liquid, or wafers in doses of 8 to 12 g/day for as long as 18 to 24 months but certainly not less than 6 months. It is often helpful to change the form of sodium bicarbonate prescribed from time to time in order to maximize patient compliance. Because of the difficulty of absorbing adequate dietary calcium, supplemental calcium gluconate should also be administered as tablets, wafers, powder, or liquid in doses of 6 to 8 g/day. As bowel adaptation progresses, the dosages of sodium bicarbonate and calcium gluconate can be reduced concomitantly or discontinued; however, such oral supplements may be necessary for 2 years or longer in some

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patients. Occasionally, on the other hand, a patient becomes severely acidotic (pH 7.0-7.2), at times as a result of increased diarrhea, but sometimes for no apparent reason, and requires urgent or emergency treatment by infusion of sodium bicarbonate IV. Usually, the patient responds promptly and completely to the therapy without untoward sequelae. Rarely, calcium gluconate must be given intravenously as an intermittent supplement to correct recalcitrant hypocalcemia «8.0 mEq/dL). Diet advancement and supplementation must obviously be individualized for best results. When solids are begun, they should be dry and followed 1 hour later with isotonic fluids to improve nutrient absorption. Lactose intolerance should be anticipated and treated with a low-lactose diet or lactase, 1 to 5 mg by mouth as needed. Obviously, milk products should be avoided as much as possible. As progress is made during the bowel adaptation period, natural fatty foods can be increased in the diet as tolerated, and supplementation with short- and medium-chain triglycerides and essential fatty acids may no longer be necessary. Serum free fatty-acid levels and triene-tetraene ratios are monitored periodically to determine the need for supplementation and the efficacy of treatment. Contrary to early reports, high-fat diets apparently are comparable to high-carbohydrate diets when evaluated in reference to calories absorbed, blood chemistry, stool or ostomy output, urine output, and electrolyte excretion.103 However, enteral intake should approach 50% to 100% greater than the expected goals to compensate for malabsorbed nutrients. 104 Patients who fail to tolerate a normal oral diet should be given a trial of constant infusion of an enteral formula. Low-residue, polymeric chemically defined or elemental diets offer the theoretical advantage of easy absorbability in these patients. However, investigators have recently shown no differences in caloric absorption, stomal output, or electrolyte losses among elemental, polymeric, and normal diets in patients with shortbowel syndrome. 50, 57, 58 Depending on the results of periodic hematologic and biochemical studies, adjustments are made in the patient's intake of sodium, potassium, chloride, and calcium. 47 Oral iron supplementation can be accomplished in the form of Fer-In-Sol 1 mL three times a day. In addition, intermittent supplemental infusions of solutions containing magnesium, zinc, and copper may be required. As malabsorption and diarrhea become less troublesome, the vitamin and trace element requirements may be satisfied by multivitamin capsules or tablets containing therapeutic dosages of vitamins and minerals (Centrum, Theragran-M), one capsule or tablet twice daily. Relatively large doses of magnesium, zinc, vitamin C, and the vitamin B complex can be administered in the form of Vicon-C, one capsule three times daily. In some patients, it may be necessary to correct individual nutrient substrate deficiencies periodically intramuscularly or intravenously for long periods of time. Intermittent infusions of human serum albumin and packed erythrocytes may be required to treat recalcitrant hypoalbuminemia and anemia and to restore the plasma albumin concentration and hematocrit to normal. Cholestyramine can be administered to combat bile salt diarrhea

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if indicated, but it must be remembered that intraluminal cholestyramine itself sometimes causes or aggravates diarrhea. Fatty acid, electrolyte, trace element, vitamin, and acid-base imbalances must be corrected enterally or parenterally as required when manifested clinically or by laboratory determination. Vitamin B12 levels must be monitored and any deficiency corrected promptly. Oxaluria should be assessed regularly, and when hyperoxaluria is present, foods containing high levels of oxalate, such as chocolate, spinach, celery, carrots, tea, and colas, should be restricted. In some patients with severe forms of short-bowel syndrome, in which little or no small bowel is present distal to the duodenum or in which the remaining small bowel has residual disease, hypermotility and recalcitrant or intractable diarrhea necessitate continuous long-term antimotility-antisecretory therapy with oral or parenteral forms and dosages of the previously described pharmacologic agents. Additional medications that have been helpful in some patients are omeprazole (Prilosec), 20 mg by mouth daily; Pro-Banthine, 15 mg by mouth every 4 to 6 hours; and Bentyl, 20 to 40' mg by mouth every 6 hours. Long-Term Management Long-term management of the short-bowel syndrome can be accomplished successfully in most patients by conscientious attention to the principles and practices already discussed. However, in a small group of patients who have undergone massive small-bowel resection, total or supplemental parenteral nutrition must be provided in a continuous or cyclic manner for extended periods of time at home, sometimes for life. The metabolic management and nutritional therapy of patients with the short-bowel syndrome must be tailored specifically to the individual patient, and the clinical responses to massive intestinal resection depend on many and varied factors, as described earlier. Patients with the shortbowel syndrome potentially pass through several stages of nutritional support during their recovery, convalescence, and rehabilitation. Ideally, they can ultimately be maintained on a normal or near-normal oral diet. However, depending on the adaptability of their residual bowel, they may have to settle for receiving their nutritional requirements via a modified oral diet, an enteral total or supplemental diet, an oral or enteral diet supplemented with intravenous fluid or electrolyte replacement, parenteral nutrition supplemented with a variable oral or enteral diet, or reliance entirely on TPN. Virtually all patients with the short-bowel syndrome eventually develop gallstones, usually necessitating cholecystectomy (and sometimes common bile duct exploration) within 2 years after the intestinal resection. Periodic abdominal ultrasonography may be useful in identifying and monitoring changes in the gallbladder and biliary tree. Finally, some otherwise-stable patients develop intractable diarrhea secondary to colonization or bacterial overgrowth of the residual small-bowel segment, requiring stool culture and parenteral treatment with appropriate antibiotics. EARLY SURGICAL MANAGEMENT Total parenteral nutrition is the mainstay of early, and sometimes late, management of the short-bowel syndrome. 23 Prior to the widespread use

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of TPN, patients often survived the initial surgical insult of massive smallbowel resection and its complications only to die ultimately of fluid, electrolyte, and nutritional imbalances. Today, however, patients usually can be managed successfully and often rehabilitated with the judicious use of TPN. In this regard, the surgeon is required to insert, maintain, and supervise a temporary or permanent indwelling central venous catheter for administration of TPN solutions. Patients with short-bowel syndrome often require surgical treatment of complications resulting from their primary illness or their operation. Abscesses may require drainage, fistulas may require excision with or without additional bowel resection, adhesive obstructions may require enterolysis and reduction, and wound dehiscences may require debridement and closure. In addition, a second look operation may be required to confirm the viability of the residual small bowel, to resect additional ischemic or gangrenous bowel, to revise an anastomosis, or to create an ostomy and distal bowel fistula. Whatever secondary surgical procedure is required, it must be performed without jeopardizing the remaining short bowel. A primary anastomosis may have been contraindicated or impossible at the time of the initial small-bowel resection, and a significant length of intestine may have been left outside the enteric stream. Significant nutritional benefit can accrue from re-establishing intestinal continuity, especially if the distal intestinal segment includes small bowel and the ileocecal valve. On the other hand, a jejunocolic anastomosis may be contraindicated if only a small amount of distal colon remains. An anastomosis between a short segment of small bowel and a short segment of distal colon will most likely result in severe intractable diarrhea, which will be much more poorly tolerated by the patient than a well-functioning end jejunostomy. As stated previously, massive small-bowel resection is associated with an increase in the secretion of gastrin and gastric acid. 18, 40. 59, 76, 87 The resulting hypersecretion can readily cause or aggravate peptic ulceration, diarrhea, and fluid and electrolyte depletion. Because the hypersecretion is thought to be hormonally mediated, truncal vagotomy and pyloroplasty have been performed in humans with good results. 1 Now that effective H2receptor blockers have been developed for clinical use, however, the surgical treatment of gastric hypersecretion is seldom indicated or required. In patients with the short-bowel syndrome, cimetidine has dramatically reduced duodenal acid and volume loads and decreased stool mass and fecal losses of sodium and potassium. 18, 44, 59 Currently, vagotomy or other acid-reducing operations should be reserved for those patients who develop complicated peptic ulceration problems resistant to conservative medical therapy.

LATE SURGICAL MANAGEMENT

General agreement exists among surgeons that adjunctive procedures for the short-bowel syndrome should not be performed at the time of the initial resectionY' 56, 84 No operative procedure to augment the bowel by

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slowing intestinal transit or increasing absorption is sufficiently safe and effective to recommend its routine use (Table 3).83 In time, intestinal adaptation or compensation frequently will result in sufficient absorption of nutrients to obviate additional surgical intervention. Moreover, there is strong evidence that performing adjunctive procedures at the time of massive small-bowel resection actually diminishes the potential for maximum bowel adaptation. 1,31, 99 In patients with the short-bowel syndrome, parenteral nutrition should be given for at least 6 to 12 months to ensure that optimal bowel adaptation has occurred before contemplating any surgical procedures to increase the absorption of nutrients. 23 In most patients, sufficient bowel adaptation occurs during the first year after the intestinal resection that parenteral nutrition can be discontinued, and the contemplated surgical intervention can be avoided. In recent years, the use of intestinal interpositions as a method of treating short-bowel syndrome surgically has generated more interest than any other operative approach. Small-bowel segments 10 to 15 cm in length are interposed at the same or a different location, usually in an antiperistaltic direction, but sometimes in an isoperistaltic direction. Segments longer than 15 cm, when reversed, can cause chronic obstruction, progressive weight loss, and even death,55 Case reports on use of reversed small-bowel segments in patients with the short-bowel syndrome have documented variable results in 18 adult patients and 5 infants,29, 35, 41, 46, 62, 83, 66, 74, 91, 99 Colonic interpositions have also been used, with inconsistent results, primarily in infants. 33, 38 The objection to using either small-intestinal or colonic reversed segments is that they both usually cause an element of intestinal obstruction. Although some delay in intestinal transit may be beneficial, the creation of a true obstruction may result in stasis, bacterial overgrowth, and an actual decrease in absorption. Although a clear mandate for the use of interposed intestinal or colonic segments cannot be derived from the reported data, such interpositions should be considered when venous access cannot be secured or maintained, or when symptomatic hepatic dysfunction develops. A technique for doubling the length of a Table 3. Alternative Surgical Strategies in Short-bowel Syndrome VALUE OPERATIVE GOAL

To decrease intestinal motility Construction of intestinal valves Antiperistaltic intestinal segments Colon interposition ReCirculating loops Intestinal pacing To decrease absorptive area Intestinal tapering and lengthening Growing neomucosa Intestinal transplantation To control gastric hyperacidity Vagotomy and pyloroplasty

Proved Questionable

None

REFERENCES

X X

53,72,90 4, 5, 22, 45, 99 33, 38, 52, 89 14, 19, 54, 66, 70, 93 23,36,37

X X X

X X X

6, 7, 9, 68, 82, 95 8,34 2, 30, 78, 79, 92

X

1, 31, 40, 69, 73

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segment of small intestine by dividing the mesentery longitudinally in the midline at its junction with the small bowel, and then dividing the bowel lengthwise using a gastrointestinal stapler, produces two intestinal tubes side by side. When the ends of these tubes are anastomosed, the lumen of the bowel is narrower, but the length is doubled. 6 Use of this technique has been reported in six children, with promising results; however, the procedure is technically demanding and has a high potential for postoperative complications secondary to anastomotic leak and obstruction. 7. 84 Currently, it can be recommended only in highly selected patients and with caution. 23 Jejunocolic valves have been created either by intussuscepting the jejunum into the colon for 4 cm 72 or by intussuscepting the colon into the distal small bowel. 90 Although artificial valves appear to be of benefit in experimental animals, their use in humans is unproven, and the risks of making the valve may outweigh the benefits. Various recirculating bowel loops have been constructed in an attempt to prolong the contact between intestinal chyme and the mucosa. The theoretical advantage of a recirculating loop over a reversed segment of small bowel is that the former promotes prolonged contact of intestinal contents with the bowel mucosa without intestinal obstruction. Surgical construction of a recirculating loop incurs the risk of multiple bowel anastomoses and has the potential for short-circuiting a portion of the intestine and thus increasing bacterial overgrowth. Because of these risks, coupled with conflicting data in animals and the lack of unequivocal supportive data in humans, this operation cannot be recommended currently.23 Growing new intestinal mucosa to increase intestinal absorption has been undertaken in animals but has not yet been attempted in humans. Incisions in the rabbit small bowel that are patched with colonic serosa or abdominal wall muscle have led to the generation of a new mucosa over the patch. 13. 51. 84. 85 The neomucosa in both the colonic serosal patches and the abdominal wall muscle patches functioned equally well. 84 When GoreTex or Dacron was used as a bed for the growth of neomucosa, the results were less impressive. 49. 94 Further work obviously needs to be done before widespread practical clinical application of this technique can be recommended. Retrograde electrical pacing slows transit through the small intestine and increases the absorption of water, glucose, and sodium in dogs with short-bowel syndromes. 37 However, when this technique was applied in one patient with short-bowel syndrome, little improvement occurred. 23 Although intestinal transplantation is the logical solution to many of the problems imposed on patients who have undergone massive smallbowel resection, rejection remains a significant obstacle. So far, all patients who have received intestinal transplants have died, and even the longest survivor never developed adequate graft function. 67 With future breakthroughs in the control of graft rejection, many patients who now require long-term TPN may benefit from successful small-bowel transplantation. 23

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PREVENTIVE SURGICAL MANAGEMENT Extensive small-bowel resections should be avoided whenever possible. Moreover, all bowel resections should be considered bowel amputations. When it is necessary to resect portions of the small bowel, the same principles should be applied as are observed when performing amputations of the extremities; that is, preserve the maximum length consistent with removing the nonviable or nonfunctioning segments or parts while maintaining optimal functions of the remaining segments or parts. Early diagnosis and treatment of mesenteric vascular insufficiency, prompt removal of clots and emboli from the mesenteric circulation, and early operation for complete bowel obstruction can help to accomplish this goal. Conservative resections of ischemic bowel together with second-look procedures to assess bowel of questionable viability should be carried out routinely. Conservative bowel resections and the judicious use of procedures such as stricturoplasty in patients with Crohn's disease can help to minimize or prevent the occurrence of short-bowel syndrome in these patients. Finally, every attempt should be made to preserve the ileocecal valve when resecting the distal or terminal ileum for any reason other than malignant disease.

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