Page 1

Nutrition in Clinical Practice

Postgastrectomy Nutrition Nutr Clin Pract 2011 26: 126 DOI: 10.1177/0884533611400070 The online version of this article can be found at:

Published by:

On behalf of:

The American Society for Parenteral & Enteral Nutrition

Additional services and information for Nutrition in Clinical Practice can be found at: Email Alerts: Subscriptions: Reprints: Permissions:

Downloaded from by Natalia Jara on May 19, 2011

Invited Review

Nutrition in Clinical Practice Volume 26 Number 2 April 2011 126-136 © 2011 American Society for Parenteral and Enteral Nutrition 10.1177/0884533611400070 hosted at

Postgastrectomy Nutrition Christie Rogers, MS, RD, CNSC Financial disclosure: none declared.

diet manipulation for symptom relief is recommended. This review highlights the physiology behind common postgastrectomy complications, provides guidelines for the medical and nutrition management of these complications, and presents a basic approach to postgastrectomy gastrointestinal symptoms.

Gastric resection, whether partial or total gastrectomy, often results in nutrition-related complications including weight loss, diet intolerances, and micronutrient deficiencies. The physiology of normal and postgastrectomy digestion is the basis for most of the current diet recommendations after gastric surgery. A careful review reveals that there is not sufficient literature to support a standard postgastrectomy diet. Rather, individualized

Keywords:   gastrectomy; nutrition therapy; nutrition support


acid production makes this surgery an option for patients with peptic ulcers that do not respond to acid-suppressing medications.1 Partial gastrectomy is also a treatment option for those with localized gastric cancer. A Billroth I or II procedure will reestablish continuity of the gastrointestinal (GI) tract. A Billroth I reconstruction, or gastroduodenostomy, involves creating an anastomosis between the distal gastric segment and the proximal duodenum (Figure 1). A Billroth II reconstruction, or gastrojejunostomy, involves making an anastomosis between the distal gastric segment and the proximal jejunum. A “blind loop” of duodenum is created to maintain the flow of bile salts and pancreatic enzymes2 (Figure 2).

he prevalence of gastric resection has decreased with improved medical management of peptic ulcer disease. Gastrectomy remains a treatment option for patients with refractory peptic ulcer disease and is the primary treatment for localized gastric cancer. Clinicians will continue to encounter patients with partial or total gastrectomies. The most common nutrition-related postgastrectomy complications include weight loss, gastric stasis, dumping syndrome, fat maldigestion, and nutrient deficiencies. Appropriate nutrition interventions can reduce or prevent these complications. Therefore, it is important for clinicians to recognize nutrition complications associated with this surgery and be knowledgeable of dietary modifications that may alleviate these complications. The traditional postgastrectomy diet, with its many restrictions, is based on well-studied physiology of anatomical changes postoperatively. A careful review of the literature reveals there is no consensus as to the optimal way to feed postgastrectomy patients. Nutrition management of these patients may need to be individualized and will require careful monitoring and adjusting based on the patient’s symptoms.

Vagotomy Vagotomy, or resection of the vagus nerve, may be completed in conjunction with a Billroth I or Billroth II reconstruction, or as a stand-alone procedure. A vagotomy eliminates cholinergic stimulation of acid-producing gastric cells.3 In a total vagotomy, the innervations to both the parietal cells and the portion of the vagus nerve that control gastric emptying are eliminated.2 This results in decreased acid production but also leads to gastric stasis and poor gastric emptying.4 To improve gastric emptying, a pyloroplasty (enlarging of the pyloric sphincter) or gastrojejunostomy may also be performed.4 In a selective, or partial, vagotomy, only the vagal nerve innervations to the parietal cells are severed, preserving the functions of the antrum and pylorus.2,4 In a partial vagotomy, acid production is decreased whereas gastric emptying and peristalsis remain functional.2

Overview of Gastric Surgeries Partial Gastrectomy A partial gastrectomy involves removal of the gastric antrum and the gastrin-producing G cells that promote hydrochloric acid secretion.1 The resultant decrease in

From the University of Virginia Health System, Nutrition Support Services, Charlottesville, Virginia

Total Gastrectomy

Address correspondence to: Christie Rogers, University of Virginia Health System, Nutrition Support Services, PO Box 800673, Charlottesville, VA 22908; e-mail:

A total gastrectomy involves the removal of the entire stomach with a Roux-en-Y reconstruction to establish GI 126

Downloaded from by Natalia Jara on May 19, 2011

Postgastrectomy Nutrition / Rogers   127

Postgastrectomy Nutrition-Related Complications Weight Loss Weight loss after partial or total gastrectomy is well documented.5-9 Pedrazzani et al8 evaluated 195 patients, over a 5-year period, who had undergone subtotal gastrectomy with Billroth II reconstruction. The authors demonstrated that the majority of weight loss occurred within the first 3 months after gastric surgery.8 Weight then stabilized and a small amount of weight gain was observed, although few patients attained preoperative weight.8 Postprandial fullness appears to contribute to weight loss, especially during the first 3-6 months after operation.8 Weight loss may also result from inadequate food intake due to dumping syndrome symptoms or due to nutrient malabsorption.10 Because the majority of weight loss appears to occur within the first 3 months postoperatively, it is important that early nutrition interventions aim to curtail this trend.8,11,12 The following sections will address the hypothesized reasons for weight loss, including gastric stasis, dumping syndrome, and fat maldigestion. Dietary modifications that may alleviate these postgastrectomy nutrition complications will be addressed. In addition, a basic approach to postgastrectomy GI complications is provided in Figure 4.

Figure 1.   Billroth I.

Figure 2.   Billroth II. Figures courtesy of CancerHelp UK:

Figure 3.   Total gastrectomy.

tract continuity. With a Roux-en-Y, the jejunum is pulled up and anastomosed to the esophagus. The duodenum is connected to the small bowel so that bile and pancreatic secretions can flow into the intestine (Figure 3). In some instances, the Roux limb is doubled over to create an artificial “stomach pouch.”4 Loss of the entire stomach results in a functional vagotomy and consequently eliminates acid production.

Gastric Stasis Patients with gastric stasis, or delayed gastric emptying, often present with nausea and vomiting, loss of appetite, bloating and fullness, or early satiety.4 Incidence of gastric stasis following gastrectomy ranges from 0.4% to 13%.4,13,14 Total vagotomy often causes gastric stasis since the loss of the vagus nerve inhibits normal gastric emptying. However, even in Billroth II procedures without vagotomy, patients have experienced gastric stasis, possibly due to hypomotility of the gastric remnant.15,16 Motor disturbances in the jejunal limb following distal and total gastrectomy may also lead to gastric stasis.16,17 Once mechanical obstruction and ulcer disease have been excluded via upper endoscopy or radiographic imaging, a gastric emptying test can be used to diagnose gastric stasis.18 Several methods exist to evaluate gastric emptying, including scintigraphy, stable isotope breath test, and ultrasonography. Gastric emptying by scintigraphy is considered the gold standard because it evaluates the emptying of a standard meal.18 This meal typically includes 2 eggs, 2 pieces of white toast, and water, so that the procedure analyzes the emptying of both liquids and solids with approximately the same distribution of calories, fat, protein, and carbohydrates.18,19 Gastric emptying is abnormal when greater than 50% of the meal is retained after 2 hours of study or when greater than 10%

Downloaded from by Natalia Jara on May 19, 2011

128   Nutrition in Clinical Practice / Vol. 26, No. 2, April 2011

Partial Gastrectomy or Total Gastrectomy

I. Procedure

II. Symptoms

III. Differential

IV. Evaluation

V. Management


Fat Malabsorption

-72 hr fecal fat

-If SBBO suspected, empirically treat with antibiotics -If SBBO not suspected, initiate a trial of pancreatic enzymes


Dumping Syndrome

-Symptom Evaluation -OGTT

-Dietary modifications (see article for details) -If symptoms continue despite diet manipulation, consider the following medications: -acarbose (most effective with late dumping syndrome) -octreotide (use only after exhausting all other options)

Early Satiety

Gastric Stasis

-Gastric Emptying by Scintigraphy

-Trial of prokinetic and/or antiemetic agents -If symptoms continue, initiate dietary modifications (see article for details)

This algorithm is intended to aid in the evaluation and management of common symptoms that occur after partial or total gastrectomy. After identifying symptoms (II), fat malabsorption, dumping syndrome, and gastric stasis can be confirmed (III) using diagnostic tools provided (IV). Guidelines for management are also included (V). Abbreviations: SBBO, small bowel bacterial overgrowth; OGTT, oral glucose tolerance test

Figure 4.   Approach to postgastrectomy GI symptoms.

of the meal is retained after 4 hours.19 During isotope breath tests, patients typically ingest eggs labeled with 13C or 14C octanoic acid.18,19 After passage into the small bowel, the labeled solid is metabolized to the labeled CO2, which is then excreted by the lungs.18,19 Breath samples are obtained every 10-15 minutes after egg ingestion to determine the time it takes for food to pass into the small bowel.18,19 Isotope breath tests have not been validated in patients with abnormal small bowel, pancreas, liver, or pulmonary function.18,19 Ultrasonography is not ideal because of operator dependence and its inability to assess the emptying of solid materials.18,19 Although breath testing and ultrasonography are not recommended as the gold standard to assess gastric emptying, they are less invasive and do not involve ionizing radiation exposure.19 Medication management of gastric stasis typically involves the use of prokinetic and antiemetic agents.20 Metoclopramide has an antiemetic and a prokinetic

effect.20 Onset of action is typically 60 minutes after an oral dose and 30 minutes after an intravenous dose.20 A usual dose of metoclopramide is 5-20 mg orally 4 times per day or 10 mg intravenously every 2-3 hours. 20 Erythromycin, both orally and intravenously, has been used to promote gastric emptying.20 Since erythromycin is typically used to address acute symptom flares, intravenous administration of 1-2 mg per kg every 8 hours is usually recommended.20 Oral dosing of 50-250 mg 4 times per day is also an option.20 Although nausea and vomiting secondary to gastric stasis typically resolve with prokinetic agents alone, antiemetics can also be used if nausea persists. Promethazine can be given orally, intramuscularly, or per rectum at a dosage of 12.5-50.0 mg every 4 to 6 hours.20 Both prokinetic and antiemetic agents are best provided in regularly scheduled doses rather than on an as-needed basis.4,20 Patients with gastric stasis have an increased risk for small bowel bacterial overgrowth (SBBO). Although

Downloaded from by Natalia Jara on May 19, 2011

Postgastrectomy Nutrition / Rogers   129

healthy bowel contains a certain amount of bacteria, the presence of an excess number of bacteria in an atypical location represents SBBO.21 Symptoms occur when the human host competes with the excessive bacteria for ingested nutrients or when the excessive bacteria cause injury to the small bowel epithelium.21 Ironically, the symptoms of SBBO can be similar to those of gastric stasis: nausea, vomiting, bloating, or early satiety.4 SBBO can be diagnosed by obtaining a small bowel aspirate during endoscopy.21 Although this is the gold standard, limitations exist.21 This process will not detect SBBO occurring in the distal small intestine. Furthermore, more than 50% of the bacterial species of the GI tract cannot be cultured, making identification of the microorganisms difficult.21 Hydrogen breath testing is an alternative and more commonly used method to diagnose SBBO.21 However, false-positive hydrogen breath tests have been seen in patients with a history of gastric resection.21 Given discrepancies and difficulties with testing and diagnosis of SBBO, it is common to empirically treat with enteral antibiotics that cover both aerobic and anaerobic bacteria. The use of probiotics for the prevention or treatment of SBBO has been postulated, but human studies are minimal and inconsistent.22-25 Additional research in this area would be beneficial. If gastric stasis is not responding to dietary and medical interventions, the presence of SBBO should be investigated and treated. Gastric stasis can also increase the incidence of bezoar formation. These accumulations of undigested material or medications within the GI tract can cause obstructions that may require surgical intervention. Like SBBO, the presence of a bezoar can mimic the classic symptoms of gastric stasis.4 Although plain abdominal radiographs and barium studies may identify a bezoar, endoscopy is the preferred method for diagnosing bezoars.26 Removal of the bezoar alone may eliminate the symptoms that were once attributed to gastric stasis. If, however, the patient developed a bezoar because of gastric stasis, dietary modifications can reduce the incidence of additional bezoars. Details regarding these modifications are discussed below. There are several dietary modifications that may alleviate the symptoms associated with gastric stasis. Prior to deciding which modification to recommend, the clinician should obtain a thorough diet history from the patient. Only 1 or 2 aspects of the diet should be changed at a time so that symptom relief can be achieved without unnecessary dietary restrictions.4 These recommendations have not been validated by controlled trials but are derived from the idea that certain foods enhance gastric emptying. Additionally, most gastric emptying studies involve nonsurgical, healthy patients. More research evaluating postgastrectomy gastroparesis and diet manipulation would be beneficial.

Nutrition Interventions for Gastric Stasis Symptoms include nausea and/or vomiting after meals. Begin by advising patient to eat smaller, more frequent meals throughout the day. Symptoms are exacerbated after eating solid foods but minimal after consuming liquids. Encourage patient to increase calories from liquids or pureed foods. Pureed foods usually empty from a gastroparetic stomach even when larger particles are retained.4,20,27 Symptoms continue despite medications and previous diet modifications. Initiate a trial of a low-fat/low-fiber diet. Lipids and indigestible fibers have been reported to delay gastric emptying.4,20,28 Liquid fats do not pose a problem and therefore should not be avoided.4 Patient with a history of bezoar formation. Encourage patients to avoid foods high in fiber, especially citrus fruits and raw vegetables. Patients should also eliminate bulk-forming laxatives, such as psyllium.26,29

Dumping Syndrome Dumping syndrome occurs when food rapidly empties into the small bowel resulting in GI and/or vasomotor symptoms. After gastric surgery, 25%-50% of patients experience dumping syndrome. Of these patients, 5%-10% experience symptoms that are clinically significant.22 Symptoms of dumping syndrome present during the first 3 months after surgery and can resolve within 1 year postoperatively.8 Although the symptoms were identified and the term dumping was coined nearly a century ago, the pathophysiology of dumping syndrome continues to be contested.30 Two forms of dumping syndrome have been observed: early and late. Early dumping syndrome occurs 10-30 minutes post prandial with a combination of GI and vasomotor symptoms.31 These may include abdominal pain, bloating, nausea, vomiting, diarrhea, headache, flushing, fatigue, and hypotension.22,31 Late dumping syndrome occurs 1-3 hours post prandial with predominantly vasomotor symptoms. Symptoms of late dumping syndrome include perspiration, weakness, confusion, shakiness, hunger, and hypoglycemia.22,31 The decreased gastric reservoir and loss of the pyloric sphincter after gastric surgery mean that food passage into the small intestine is accelerated. Typically, the antrum grinds food particles into 1-2 mm fragments before delivery into the small intestine.31 Without the stomach sieving or grinding, large, difficult-to-digest particles are funneled into the small intestine.32 Early dumping syndrome GI symptoms most likely occur because of

Downloaded from by Natalia Jara on May 19, 2011

130   Nutrition in Clinical Practice / Vol. 26, No. 2, April 2011

the rapid influx of hyperosmolar contents into the duodenum or small intestine.22,31 A subsequent fluid shift from the intravascular compartment to the intestinal lumen is observed. This results in small intestine distention, which may cause cramps and bloating.22,31 The vasomotor symptoms of early dumping have been attributed to elevated serotonin levels.10,33 Serotonin as a neurotransmitter causes vasodilation manifested as flushing, hypotension, and increased gastric motility, the symptoms associated with early dumping. Late dumping syndrome is most likely the result of reactive hypoglycemia. Because of the surgical changes previously explained, large amounts of carbohydrate are delivered rapidly into the small intestine. This causes an accelerated absorption of glucose into the blood.22 Subsequently, excessive insulin is released and a reactive hypoglycemic response is observed.22,34,35 Glucagon-like peptide-1 (GLP-1) is also involved in late dumping syndrome. The secretion of GLP-1 from the small intestine and colon results in insulin release.22,36 Several studies have demonstrated an increase in GLP-1 secretion following an oral glucose challenge in patients who have had gastric resection.22,37-39 Dumping syndrome is typically confirmed by the presence of the previously mentioned symptoms in a patient with a history of upper abdominal surgery.22,31 Hypoglycemia combined with several GI symptoms is strongly indicative of dumping syndrome.31 An oral glucose tolerance test using a 50-75 g glucose solution after an overnight fast can be used to confirm dumping syndrome.31 Blood glucose, hematocrit, pulse rate, and blood pressure are measured immediately before glucose ingestion and every 30 minutes for up to 180 minutes after ingestion.31 The test is considered positive if hypoglycemia occurs at 120-180 minutes, if hematocrit increases by more than 3% at 30 minutes, or if pulse rate increases by more than 10 beats per minute at 30 minutes. Patients with refractory dumping syndrome, despite diet manipulation, may benefit from pharmacologic therapy. Acarbose has been used in the treatment of late dumping syndrome because of its effect on postprandial hypoglycemia.22 Acarbose minimizes reactive hypoglycemia by delaying the conversion of polysaccharides to monosaccharides and thereby decreasing postprandial glucose and insulin release.22 A few small studies, giving 50-100 mg of acarbose to patients with late dumping syndrome, have demonstrated conflicting results.31,40-44 In a double-blind study of 9 gastric surgery patients, Speth et al42 showed improved symptoms of postprandial hypoglycemia when 50 mg of acarbose was given after a carbohydrate-rich meal. In contrast, Lyons et al43 showed no significant improvement in symptoms when 13 patients were given 50 mg of acarbose both before 1 meal and also 3 times daily before meals for 1 month. Hasegawa et al44 gave 6 gastric surgery patients with late

dumping syndrome and non–insulin-dependent diabetes mellitus 50 mg of acarbose 3 times daily before meals for 1 month. All patients demonstrated a resolution of symptoms.44 Larger, long-term prospective studies are necessary to evaluate the effect of acarbose on late dumping syndrome symptoms. Additionally, as the unabsorbed carbohydrates reach the small intestine, bacterial fermentation causes diarrhea, bloating, and flatulence.31 These side effects of acarbose may decrease patient compliance. Octreotide, a somatostatin synthetic analog, has been used in the treatment of both early and late severe dumping syndrome.22 Somatostatin analogs can delay gastric emptying and small bowel transit time, inhibit GI hormone and insulin secretion, decrease postprandial vasodilation, and increase the absorption of water and sodium in the intestine.22,31 Short-acting and long-acting repeatable (LAR) octreotide formulations have been used in the management of severe or refractory dumping syndrome. An initial dose of the short-acting formulation is a 25-50 mcg subcutaneous injection given 15-30 minutes before meals.22 If ineffective, this dose can be increased to 100 mcg.22,31 Given its slow release, the LAR octreotide formulation can be given monthly via a 20 mg intramuscular injection.31 A systematic review of randomized controlled trials evaluating the effectiveness of short-acting octreotide confirmed that octreotide, both short term and long term, improves dumping syndrome symptoms.45 However, the studies evaluated were small: 7 studies with a combined total of 63 patients.45 Several studies reported increased diarrhea with short-acting octreotide,46-48 and 2 reported steatorrhea.48,49 Despite steatorrhea, Geer et al48 reported an 11% increase in mean body weight and Vecht et al49 reported an average weight gain of 2.4 kg.22 Two studies, both open-label and uncontrolled, evaluated LAR octreotide for the treatment of dumping syndrome.50,51 Penning et al51 gave 12 patients, who previously required daily short-acting octreotide, 10-20 mg of the LAR formulation, monthly, for 6 months.51 Significant improvement in quality of life, specifically in the GI symptoms subscale, was observed in patients receiving the 10 mg dose.51 It is important to note that the 10 mg dose of LAR octreotide is not available in most countries.31 Arts et al50 gave 30 patients 50 mcg injections of short-acting octreotide 3 times daily for 3 days. On the evening of day 3, the patients were started on 20 mg of LAR octreotide intramuscularly, monthly, for 3 months.50 Both the shortacting and LAR formulations improved both early and late dumping syndrome symptoms, but the short-acting formulation alleviated late dumping symptoms better than the LAR formulation.50 The LAR formulation was associated with an improvement in quality of life.50 Further study, including large, long-term randomized controlled trials, is required to evaluate the efficacy of both short-acting and LAR octreotide in the management of dumping syndrome. The adverse effects of pain at the

Downloaded from by Natalia Jara on May 19, 2011

Postgastrectomy Nutrition / Rogers   131

site of injection, gallstone formation, increased diarrhea, and steatorrhea along with the increased cost of octreotide should all be considered before initiating this medication for dumping syndrome.31 Patients should be advised of the following dietary modifications, which may alleviate the symptoms associated with both early and late dumping syndrome. Similar to the recommendations for gastric stasis, most guidelines for the dietary management of dumping syndrome are not validated by controlled trials. Recommendations are based on the physiology of digestion and on results from gastric emptying studies. More research evaluating postgastrectomy dumping syndrome and diet manipulation would be beneficial.

intake of simple sugars decreases the delivery of hypertonic solutions to the small intestine. Eat protein at each meal. Decreasing carbohydrate intake tends to lead to a net loss of overall caloric intake. Increasing protein can offset this imbalance and help avoid unintentional weight loss. Increase intake of fiber. Gastrointestinal scintigraphy has shown that indigestible residue empties slower than both liquids and solids.19 Supplemental fibers such as guar gum, pectin, and glucomannan increase food viscosity and bind with carbohydrates to both increase transit time and slow glucose absorption.27,22,54,55

Nutrition Interventions for Dumping Syndrome

Fat Maldigestion Eat smaller, more frequent meals. Because gastric emptying is accelerated and the gastric reservoir is smaller, food passes more quickly from the stomach to the small intestine. Eating smaller meals decreases the likelihood that large amounts of food will reach the small bowel too quickly. Chew all foods thoroughly and eat slowly. With the antrum removed, the stomach can no longer grind large particles of food before passing food into the small intestine. Chewing food into smaller particles can stop the flow of large, difficult-to-digest particles into the small intestine. By decreasing the rate of food intake, one can consciously slow the passage of food to the small bowel, similar to the unconscious approach that was once managed by the pylorus. Limit fluid consumption with meals and wait at least 30 minutes after meals to drink fluid. After vagotomy, diarrhea can be increased with liquid meals, and intestinal motility can be decreased with dry meals.52 Normally, the gastric fundus creates a pressure gradient that helps control liquid emptying. Gastrointestinal scintigraphy has shown that liquids empty more quickly than solids, even in patients who have not undergone gastrectomy.19 Therefore, in a postsurgical patient, liquid passage to the small bowel may be accelerated, causing diarrhea.19 Maes et al53 evaluated the emptying of the liquid, solid, and oil phases of a meal in 7 Billroth II subjects compared with 10 normal subjects. This small study found that the solid phase emptied concurrently with the liquid phase in Billroth II subjects, whereas the solid phase emptied significantly later than the liquid phase in normal subjects.53 Limit high-sugar foods and beverages. Simple carbohydrates are hydrolyzed into osmotically active substances more quickly than are proteins and fats.10 Decreasing the

After partial or total gastrectomy, patients may experience increased fecal fat excretion. About 10% of these patients exhibit clinically significant steatorrhea.4,10,56 Symptoms of fat malabsorption are typically cramping, abdominal pain, and a greasy, foul-smelling diarrhea.2 Several mechanisms have been explored to account for fat maldigestion after gastrectomy, including decreased gastric lipase, exocrine pancreatic insufficiency, pancreatocibal asynchrony, altered cholecystokinin release, and SBBO.10,56,57 Diagnosis of steatorrhea involves the ingestion of 100 g of fat per day for 72 hours with a concurrent analysis of fecal fat excretion. A quantitative fecal fat ≤ 7 g is expected with normal fat absorption.10 In a normal stomach, chief cells in the fundus secrete gastric lipase. Lipase initiates preliminary lipid digestion.1,10 Additionally, with an intact digestive tract, gastric lipase activity increases to compensate for inadequate pancreatic lipase, thus ensuring functional lipid digestion.1 Decreased gastric lipase after subtotal or total gastrectomy results in fat malabsorption because both preliminary and compensatory lipid digestion are altered. Controversy exists regarding exocrine pancreatic insufficiency and fat malabsorption after gastrectomy. Several studies report increased fecal fat excretion following gastrectomy,5,56,58 and additional studies report decreased exocrine pancreatic function following total gastrectomy.59,60 However, studies are lacking that correlate decreased exocrine pancreatic function with steatorrhea. In a small, double-blind, crossover trial with 15 patients, Armbrecht et al61 demonstrated a statistically significant improvement in fecal fat excretion following pancreatic enzyme therapy. However, this improvement was only seen in patients who originally presented with severe steatorrhea. A follow-up prospective, double-blind, randomized, parallel, placebo-controlled, multicenter trial found that high-dose pancreatic enzyme supplementation did not significantly improve fat malabsorption in patients with total

Downloaded from by Natalia Jara on May 19, 2011

132   Nutrition in Clinical Practice / Vol. 26, No. 2, April 2011

gastrectomy.62 Not entirely consistent with the first study, all participants in the follow-up study had symptoms that were mild.62 Another study reported improvement in fecal fat excretion after adding exogenous pancreatic enzymes but only in 2 study participants with severe diarrhea.58 Sufficient evidence does not exist linking exogenous pancreatic enzymes with a specific patient benefit.63 However, from these studies a common thread emerges. Participants with severe diarrhea benefit from exogenous pancreatic enzymes, but those with minimal diarrhea do not respond to exogenous pancreatic enzymes. Additional research in this area would be beneficial to determine the utility of pancreatic enzyme supplementation in postgastrectomy patients. Another complication of gastrectomy is pancreatocibal asynchrony. The rapid transit of food through the small intestine or the bypass of the duodenum causes insufficient mixing of food with enzymes, or pancreatocibal asynchrony.56,62 With an intact GI tract, lipids empty into the small intestine more slowly than other contents. Fats leave the body of the stomach last because they form an oily layer that sits atop other gastric contents. Also, as fat reaches the duodenum, cholecystokinin is released, significantly decreasing the rate of gastric emptying.1 Maes et al53 compared gastric emptying rates of the liquid, solid, and oil phases of a meal in both normal subjects and subjects with Billroth II gastrojejunostomies. The investigators found that in normal subjects, the oil phase emptied much more slowly than the liquid phase, but in subjects with Billroth II gastrojejunostomies, in the presence of liquids the oil phase emptied extremely quickly.53 With high-calorie lipids emptying too quickly, the pancreatic enzymes released are not given sufficient time to mix with the lipids, resulting in fat malabsorption. In patients in whom this is suspected, exogenous pancreatic enzymes would be beneficial.56 As previously mentioned, SBBO can result from gastric stasis, but it can also be present in surgical blind loops.4 Stasis in these areas can lead to infection.56 Fat malabsorption occurs in patients with SBBO primarily because excess bacteria in the small bowel deconjugate bile salts and alter micelle formation.4 If fat maldigestion is the result of SBBO, deficiency of fat-soluble vitamins A, D, and E may be present.21 Vitamin K deficiency is rare in SBBO because enteric microbiota produce some micronutrients, including vitamin K, biotin, and folate.21 Patients with surgical blind loops who present with steatorrhea should be evaluated for SBBO. Diagnosis and treatment of SBBO was discussed in the section addressing gastric stasis. Nutrition Interventions for Fat Maldigestion After confirming steatorrhea with a quantitative fecal fat test and ensuring that SBBO is not to blame for fat malabsorption, the following interventions may be initiated.

Monitor and replace fat-soluble vitamins, A, D, E, and K as needed Concurrently, initiate a trial of exogenous pancreatic enzymes. Start with 500 units of lipase per kg of body weight with each meal and titrate up to desired effect. Typically, half the dosage given with meals should be taken with snacks. If steatorrhea continues, initiate a low-fat diet with medium-chain triglyceride (MCT) oil. When all possible causes of fat malabsorption have been addressed and the use of exogenous pancreatic enzymes has failed, this can be used as a last resort. The increased cost and decreased palatability of MCT oil may result in patient noncompliance.3 MCT oil contains 8.3 kcal/g, so that 15 mL, or 1 tablespoon, provides 115 kcal.64 Too much MCT oil may increase GI distress; therefore, doses of 4-5 tablespoons, administered throughout the day, are recommended.64 If a patient’s only fat source is MCT oil, essential fatty acid deficiency (EFAD) can develop. Providing 2%-4% of the patient’s total caloric intake via linoleic acid will deter EFAD.64 For example, on a 2,000-kcal diet, 40-80 kcal of linoleic acid should be recommended.64 Examples of oils containing linoleic acid include safflower oil, sunflower oil, and corn oil.64

Nutrient Deficiencies Anemia Anemia arises after partial or total gastrectomy due to vitamin B12, folate, and/or iron deficiencies. These deficiencies can result from both inadequate intake and malabsorption. It is essential to continually monitor for anemia as it can present several years after gastrectomy. Two components necessary for vitamin B12 absorption are lost with the removal of part or all of the stomach: gastric acid and intrinsic factor. Gastric acid cleaves B12 from protein whereas intrinsic factor forms a necessary complex with B12 before its absorption in the terminal ileum.65 In some cases, the duodenum and jejunum begin to produce intrinsic factor, but supplementation of B12 may still be necessary.66 Vitamin B12 deficiency also occurs in the presence of SBBO. It is postulated that bacterial use of B12 results in an insufficient amount of B12 available for absorption. Another theory suggests that bacteria produce a toxin that inhibits the transfer of B12 across the small bowel mucosa.56 Traditionally, vitamin B12 deficiency is treated with intramuscular injections. However, Adachi et al66 compared oral and intramuscular administration of supplemental B12 and found that enteral administration rapidly increased serum B12 concentration. The decision whether to supplement via oral or intramuscular route

Downloaded from by Natalia Jara on May 19, 2011

Postgastrectomy Nutrition / Rogers   133

should be based on patient comfort and compliance. Parenteral B12 supplementation begins with 1,000 mcg every day for 1 week, followed by 1,000 mcg every week for 4 weeks. To maintain normal B12 levels, monthly 1,000 mcg injections may be required for life. Oral B12 supplementation requires 1,000-2,000 mcg daily.67 Little information exists regarding folate deficiency after partial or total gastrectomy. Although folate is absorbed in the proximal small bowel and rapid transit through this area is possible after gastrectomy, folate deficiency due to malabsorption has not been documented. If suspected, folate deficiency should be diagnosed with red blood cell folate, not serum folate.4 To correct folate deficiency, 5 mg of folate should be given daily.4 Vitamin B12 is needed to activate folate, so supplementing folate with a concurrent B12 deficit will only exacerbate the B12 deficiency.68 Tovey et al5 found that 10 years after gastrectomy, iron deficiency was the most common nutrient deficiency. Iron deficiency usually occurs 10 years before the onset of B12 deficiency.5 Most iron absorption occurs along the duodenal and upper jejunum mucosa.69 After gastrectomy, bypass of the duodenum and/or rapid transit of food particles through the intestine can lead to iron deficiency.65 Additionally, gastric acid aids the conversion of ferric ions to ferrous ions, which are more easily absorbed.69 The decreased acid production following gastrectomy impedes this process. Serum ferritin, a storage protein for iron, will accurately reflect iron stores in a nonacute phase setting.3,70 Iron deficiency is best treated with 200 mg of oral elemental iron daily. A 200-mg tablet of ferrous sulfate provides 67 mg of elemental iron. Therefore, it should be given 3 times per day, 6 hours apart, and with the addition of vitamin C to enhance absorption.3,68 One case report revealed villi flattening on jejunal biopsies in a patient with anemia unresponsive to oral iron therapy. After the administration of parental iron over 4 weeks, the villous atrophy resolved and the patient’s anemia continued to improve with the use of oral iron supplementation.69 Patient compliance is often an issue with iron therapy because of side effects including nausea, abdominal pain, constipation, or diarrhea.3 Consequently, frequent encouragement to increase intake of iron-rich foods may be necessary. The heme form of iron is more available than the nonheme form of iron. Absorption of nonheme iron is enhanced by ascorbic acid (vitamin C) and amino acids and inhibited by phosphates, phytates, oxalates, and tannates.69 Heme and nonheme iron are found in meat, fish, and poultry. However, only nonheme iron exists in eggs, grains, vegetables, and fruits.71

osteopenia in 44% of Billroth I patients, 27% of Billroth II patients, and 44% of total gastrectomy patients. Bisballe et al73 found that 18% of postgastrectomy patients had osteomalacia. However, when Liedman et al74 compared total gastrectomy patients with age- and sex-matched controls, they could not demonstrate any divergence. Even though 25% of the total gastrectomy patients had osteoporosis approximately 8 years after surgery, the results indicate that this is more likely due to aging rather than a consequence of postsurgical sequelae.74 Although the cause of bone disease following gastrectomy is also unclear, several mechanisms have been suggested. Decreased dietary intake of calcium and vitamin D may play a role.3,10 Malabsorption of calcium may also be a factor because calcium is primarily absorbed in the duodenum, which may be bypassed because of surgical reconstruction or rapid transit.75 Additionally, fat malabsorption may lead to the formation of insoluble calcium soaps.75 Alterations in bone-related hormones may lead to bone disease although serum parathyroid hormone levels in postgastrectomy patients have ranged from subnormal to normal.75 Malabsorption of vitamin D has been discussed as a possible mechanism, but neither calcium nor vitamin D malabsorption has been proven in postgastrectomy patients.75 In fact, when Bisballe et al73 found osteomalacia in 18% of postgastrectomy patients, the majority if the patients had normal serum calcium and 25-hydroxyvitamin D levels (25-OHD).3 Despite the contradictions regarding incidence and cause of bone disease post gastrectomy, monitoring bone mineral density via dual-emission X-ray absorptiometry scans and ensuring that postgastrectomy patients consume adequate amounts of calcium rich foods is beneficial. This is especially true given that the majority of these surgical patients are elderly. For patients with confirmed bone disease, 1,500 mg of calcium daily is recommended.3 Additionally, as more information emerges regarding suboptimal 25-OHD levels in the healthy population, monitoring serum 25-OHD post gastrectomy seems reasonable. The current guidelines from the Institute of Medicine recommend a 25-OHD level of 20 ng/mL to maintain good bone health.76 For men and women under the age of 51, 600 international units of vitamin D daily should be sufficient to meet this goal.76 For those over the age of 71, 800 international units of vitamin D daily is recommended.76 The Institute of Medicine cautions that the risk for harm increases in doses of vitamin D beyond 4,000 international units daily.76

Implications for Clinical Practice Most studies analyzing patients post gastrectomy, including those cited in this review, have a small sample size, and few involve randomized controlled trials.* Additionally,

Bone Disease The incidence and cause of bone disease after subtotal or total gastrectomy are not clear. Zittel et al72 reported

*5, 9, 16, 53, 62, 66, 74, 77, 78

Downloaded from by Natalia Jara on May 19, 2011

134   Nutrition in Clinical Practice / Vol. 26, No. 2, April 2011

most recent studies that evaluate postgastrectomy outcomes compare different surgical procedures, not different diet approaches.11,79-81 To my knowledge, no study has compared weight loss, GI symptoms, or nutrient deficiencies in patients on a specific postgastrectomy diet versus a regular diet. Before a standard postgastrectomy diet can be proposed, more research comparing the effects of a regular diet versus a postgastrectomy diet is needed. In general, diet restrictions can increase weight loss and even make weight gain difficult. As clinicians, we must acknowledge our limitations regarding postsurgical weight gain. Copland et al77 had a registered dietitian follow postgastrectomy patients for 1 year, during which time the patients did not realize significant weight gain. Patients had difficulty increasing energy intake because they were following earlier diet restrictions. Furthermore, the patients stated that multiple diet manipulations proved burdensome.77 Given that weight loss, especially in the first 3 months after surgery, is a well-documented outcome following partial or total gastrectomy, it seems advantageous to avoid nutrition advice that may accelerate this process.5-9 Overall, there is limited evidence supporting a standard postgastrectomy diet, short-term or long-term. Diet manipulation should be individualized for symptom relief. Food restrictions should be minimal to avoid an unnecessary calorie deficit. Nutrient deficiencies should be monitored and supplemented accordingly, but excess vitamin and mineral recommendations beyond those of a standard multivitamin are not required for all postgastrectomy patients. Regular follow-up with a registered dietitian, especially during the first year after surgery, would be advantageous. However, clinicians must recognize that too many recommendations may be burdensome to the patient. As GI symptoms change or improve, appropriate diet modifications should be suggested and evaluated for effectiveness. This could avoid unnecessary diet restriction, which may exacerbate nutrient deficiencies, weight loss, and overall frustration.

References 1. Berne RM, Levy MN, Koeppen BM, Stanton BA, eds. Physiology. 5th ed. St. Louis, Mo: Elsevier, 2004. 2. Nelms M, Sucher K, Long S. Nutrition Therapy and Pathophysiology. Belmont, Calif: Thomson Brooks/Cole; 2007. 3. Radigan AE. Postgastrectomy: managing the nutrition fall-out. Pract Gastroenterol. 2004;XXVII:63-75.* 4. Rees Parrish C, Krenitsky J, Willcutts K, Radigan AE. Gastrointestinal disease. In: Gottschlich M, DeLegge M, Mattox T, Mueller C, Worthington P, Guenter P, eds. The A.S.P.E.N. Nutrition Support Core Curriculum: A Case-Based Approach— The Adult Patient. Silver Spring, Md: American Society for Parenteral and Enteral Nutrition; 2007:508-539. 5. Tovey FI, Godfrey JE, Lewin MR. A gastrectomy population: 25-30 years on. Postgrad Med J. 1990;66:450-456. 6. Bozzetti F, Ravera E, Cozzaglio L, et al. Comparison of nutrition status after total or subtotal gastrectomy. Nutrition. 1990;6:371-375.

7. Staël von Holstein C, Walther B, Ibrahimbegovic E, Akesson B. Nutrition status after total and partial gastrectomy with Roux-en-Y reconstruction. Br J Surg. 1991;78:1084-1087. 8. Pedrazzani C, Marrelli D, Rampone B, et al. Postoperative complications and functional results after subtotal gastrectomy with Billroth II reconstruction for primary gastric cancer. Dig Dis Sci. 2007;52:1757-1763. 9. Speicher JE, Thirlby RC, Burggraaf J, Kelly C, Levasseur S. Results of completion gastrectomies in 44 patients with postsurgical gastric atony. J Gastrointest Surg. 2009;13:874-880. 10. Beyer P. Medical nutrition therapy for upper gastrointestinal tract disorders. In: Mahan LK, Escott-Stump S, eds. Krause’s Food Nutrition and Diet Therapy. 11th ed. Philadelphia, Pa: Elsevier; 2004:686-704. 11. Svedlund J, Sullivan M, Liedman B, Lundell L, Sjodin I. Quality of life after gastrectomy for gastric carcinoma: controlled study of reconstructive procedures. World J Surg. 1997;21:422-433. 12. Liedman B, Andersson H, Berglund B, et al. Food intake after gastrectomy for gastric carcinoma: the role of a gastric reservoir. Br J Surg. 1996;83:1138-1143. 13. Dong K, Yu XJ, Li B, Wen EG, Xiong W, Guan QL. Advances in mechanisms of postsurgical gastroparesis syndrome and its diagnosis and treatment. Chin J Dig Dis. 2006;7:76-82. 14. Soykan I, Sivri B, Sarosiek I, Kiernan B, McCallum RW. Demography, clinical characteristics, psychological and abuse profiles, treatment, and long-term follow-up of patients with gastroparesis. Dig Dis Sci. 1998;43:2398-2404. 15. Schaap HM, Smout AJ, Akkermans LM. Myoelectrical activity of the Billroth II gastric remnant. Gut. 1990;31:984-988. 16. Le Blanc-Louvry I, Savoye G, Maillot C, Denis P, Ducrotte P. An impaired accommodation of the proximal stomach to a meal is associated with symptoms after distal gastrectomy. Am J Gastroenterol. 2003;98:2642-2647. 17. Le Blanc-Louvry I, Ducrotte P, Peillon C, Michel P, Chiron A, Denis P. Roux-en-Y limb motility after total or distal gastrectomy in symptomatic and asymptomatic patients. J Am Coll Surg. 2000;190:408-417. 18. Park MI, Camilleri M. Gastroparesis: clinical update. Am J Gastroenterol. 2006;101:1129-1139. 19. Maurer AH, Parkman HP. Update on gastrointestinal scintigraphy. Semin Nucl Med. 2006;36:110-118. 20. Rabine JC, Barnett JL. Management of the patient with gastroparesis. J Clin Gastroenterol. 2001;32:11-18. 21. DiBaise JK. Nutrition consequences of small intestinal bacterial overgrowth. Pract Gastroenterol. 2008;XXXII:15-28.* 22. Ukleja A. Dumping syndrome: pathophysiology and treatment. Nutr Clin Pract. 2005;20:517-525. 23. Quigley EM, Quera R. Small intestinal bacterial overgrowth: roles of antibiotics, prebiotics, and probiotics. Gastroenterology. 2006; 130(2 suppl 1):S78-90. 24. Vanderhoof JA, Young RJ, Murray N, Kaufman SS. Treatment strategies for small bowel bacterial overgrowth in short bowel syndrome. J Pediatr Gastroenterol Nutr. 1998;27:155-160. 25. Attar A, Flourie B, Rambaud JC, Franchisseur C, Ruszniewski P, Bouhnik Y. Antibiotic efficacy in small intestinal bacterial overgrowth-related chronic diarrhea: a crossover, randomized trial. Gastroenterology. 1999;117:794-797. 26. Sanders MK. Bezoars: from mystical charms to medical and nutrition management. Pract Gastroenterol. 2004;XXVIII:37-50.* 27. Karamanolis G, Tack J. Nutrition and motility disorders. Best Pract Res Clin Gastroenterol. 2006;20:485-505. 28. Abell TL, Camilleri M, Donohoe K, et al. Consensus recommendations for gastric emptying scintigraphy: a joint report of the American Neurogastroenterology and Motility Society and the Society of Nuclear Medicine. J Nucl Med Technol. 2008;36:44-54. 29. Emerson AP. Foods high in fiber and phytobezoar formation. J Am Diet Assoc. 1987;87:1675-1677.

Downloaded from by Natalia Jara on May 19, 2011

Postgastrectomy Nutrition / Rogers   135 30. Hertz AF. IV. The cause and treatment of certain unfavorable aftereffects of gastro-enterostomy. Ann Surg. 1913;58:466-472. 31. Tack J, Arts J, Caenepeel P, De Wulf D, Bisschops R; Medscape. Pathophysiology, diagnosis and management of postoperative dumping syndrome. Nat Rev Gastroenterol Hepatol. 2009;6:583-590. 32. Mayer EA, Thompson JB, Jehn D, Reedy T, Elashoff J, Meyer JH. Gastric emptying and sieving of solid food and pancreatic and biliary secretion after solid meals in patients with truncal vagotomy and antrectomy. Gastroenterology. 1982;83(1 pt 2):184-192. 33. Johnson LP, Sloop RD, Jesseph JE, Harkins HN. Serotonin antagonists in experimental and clinical “dumping”. Ann Surg. 1962;156:537-549. 34. Andreasen JJ, Orskov C, Holst JJ. Secretion of glucagon-like peptide-1 and reactive hypoglycemia after partial gastrectomy. Digestion. 1994;55:221-228. 35. Shultz KT, Neelon FA, Nilsen LB, Lebovitz HE. Mechanism of postgastrectomy hypoglycemia. Arch Intern Med. 1971;128: 240-246. 36. Naslund E, Bogefors J, Skogar S, et al. GLP-1 slows solid gastric emptying and inhibits insulin, glucagon, and PYY release in humans. Am J Physiol. 1999;277(3 pt 2):R910-916. 37. Schattenmann G, Ebert R, Siewert R, Creutzfeldt W. Different response of gastric inhibitory polypeptide to glucose and fat from duodenum and jejunum. Scand J Gastroenterol. 1984;19:260-266. 38. Miholic J, Orskov C, Holst JJ, Kotzerke J, Pichlmayr R. Postprandial release of glucagon-like peptide-1, pancreatic glucagon, and insulin after esophageal resection. Digestion. 1993;54:73-78. 39. Miholic J, Orskov C, Holst JJ, Kotzerke J, Meyer HJ. Emptying of the gastric substitute, glucagon-like peptide-1 (GLP-1), and reactive hypoglycemia after total gastrectomy. Dig Dis Sci. 1991;36:1361-1370. 40. McLoughlin JC, Buchanan KD, Alam MJ. A glycoside-hydrolase inhibitor in treatment of dumping syndrome. Lancet. 1979;2: 603-605. 41. Gerard J, Luyckx AS, Lefebvre PJ. Acarbose in reactive hypoglycemia: a double-blind study. Int J Clin Pharmacol Ther Toxicol. 1984;22:25-31. 42. Speth PA, Jansen JB, Lamers CB. Effect of acarbose, pectin, a combination of acarbose with pectin, and placebo on postprandial reactive hypoglycaemia after gastric surgery. Gut. 1983;24:798802. 43. Lyons TJ, McLoughlin JC, Shaw C, Buchanan KD. Effect of acarbose on biochemical responses and clinical symptoms in dumping syndrome. Digestion. 1985;31:89-96. 44. Hasegawa T, Yoneda M, Nakamura K, et al. Long-term effect of alpha-glucosidase inhibitor on late dumping syndrome. J Gastroenterol Hepatol. 1998;13:1201-1206. 45. Li-Ling J, Irving M. Therapeutic value of octreotide for patients with severe dumping syndrome--a review of randomised controlled trials. Postgrad Med J. 2001;77:441-442. 46. Hopman WP, Wolberink RG, Lamers CB, Van Tongeren JH. Treatment of the dumping syndrome with the somatostatin analogue SMS 201-995. Ann Surg. 1988;207:155-159. 47. Primrose JN. Octreotide in the treatment of the dumping syndrome. Digestion. 1990;45(suppl 1):49-58; discussion 58-89. 48. Geer RJ, Richards WO, O’Dorisio TM, et al. Efficacy of octreotide acetate in treatment of severe postgastrectomy dumping syndrome. Ann Surg. 1990;212:678-687. 49. Vecht J, Lamers CB, Masclee AA. Long-term results of octreotidetherapy in severe dumping syndrome. Clin Endocrinol (Oxf). 1999;51:619-624. 50. Arts J, Caenepeel P, Bisschops R, et al. Efficacy of the long-acting repeatable formulation of the somatostatin analogue octreotide in postoperative dumping. Clin Gastroenterol Hepatol. 2009;7:432-437.

51. Penning C, Vecht J, Masclee AA. Efficacy of depot long-acting release octreotide therapy in severe dumping syndrome. Aliment Pharmacol Ther. 2005;22:963-969. 52. McKelvey ST. Gastric incontinence and post-vagotomy diarrhoea. Br J Surg. 1970;57:741-747. 53. Maes BD, Hiele MI, Geypens BJ, Ghoos YF, Rutgeerts PJ. Gastric emptying of the liquid, solid and oil phase of a meal in normal volunteers and patients with Billroth II gastrojejunostomy. Eur J Clin Invest. 1998;28:197-204. 54. Harju E, Larmi TK. Efficacy of guar gum in preventing the dumping syndrome. JPEN J Parenter Enteral Nutr. 1983;7:470-472. 55. Hopman WP, Houben PG, Speth PA, Lamers CB. Glucomannan prevents postprandial hypoglycaemia in patients with previous gastric surgery. Gut. 1988;29:930-934. 56. Grant JP, Chapman G, Russell MK. Malabsorption associated with surgical procedures and its treatment. Nutr Clin Pract. 1996;11: 43-52. 57. Sategna-Guidetti C, Bianco L. Malnutrition and malabsorption after total gastrectomy: a pathophysiologic approach. J Clin Gastroenterol. 1989;11:518-524. 58. Bae JM, Park JW, Yang HK, Kim JP. Nutrition status of gastric cancer patients after total gastrectomy. World J Surg. 1998;22:254260; discussion 260-261. 59. Friess H, Bohm J, Muller MW, et al. Maldigestion after total gastrectomy is associated with pancreatic insufficiency. Am J Gastroenterol. 1996;91:341-347. 60. Fischermann K, Harly S, Worning H, Zacho A. Pancreatic function and the absorption of fat, iron, vitamin B12, and calcium after total gastrectomy for gastric cancer. Gut. 1967;8:260-266. 61. Armbrecht U, Lundell L, Stockbrugger RW. The benefit of pancreatic enzyme substitution after total gastrectomy. Aliment Pharmacol Ther. 1988;2:493-500. 62. Bragelmann R, Armbrecht U, Rosemeyer D, Schneider B, Zilly W, Stockbrugger RW. The effect of pancreatic enzyme supplementation in patients with steatorrhoea after total gastrectomy. Eur J Gastroenterol Hepatol. 1999;11:231-237. 63. Griffiths A, Taylor RH. Postgastrectomy pancreatic malabsorption: is there a case for intervention? Eur J Gastroenterol Hepatol. 1999; 11:219-221. 64. McCray S, Rees Parrish C. When chyle leaks: nutrition management options. Pract Gastroenterol. 2004;XXVIII:60-76.* 65. Fernandez-Banares F, Monzon H, Forne M. A short review of malabsorption and anemia. World J Gastroenterol. 2009;15:4644-4652. 66. Adachi S, Kawamoto T, Otsuka M, Todoroki T, Fukao K. Enteral vitamin B12 supplements reverse postgastrectomy B12 deficiency. Ann Surg. 2000;232:199-201. 67. Stanley SL. Diagnosis and treatment of vitamin B12 and folic acid deficiency. .do?topicKey=red_cell/6632&selectedTitle=1%7E22&source=sea rch_result. Updated 2010. Accessed September 30, 2010. 68. Pawson R, Mehta A. Review article: the diagnosis and treatment of haematinic deficiency in gastrointestinal disease. Aliment Pharmacol Ther. 1998;12:687-698. 69. Lizarraga A, Cuerda C, Junca E, et al. Atrophy of the intestinal villi in a postgastrectomy patient with severe iron deficiency anemia. Nutr Hosp. 2009;24:618-621. 70. Carlson TH. Laboratory data in nutrition assessment. In: Mahan LK, Escott-Stump S, eds. Krause’s Food Nutrition and Diet Therapy. 11th ed. Philadelphia, Pa: Elsevier; 2004:436-454. 71. Stopler T. Medical nutrition therapy for anemia. In: Mahan LK, Escott-Stump S, eds. Krause’s Food Nutrition and Diet Therapy. 11th ed. Philadelphia, Pa: Elsevier; 2004:838-859. 72. Zittel TT, Zeeb B, Maier GW, et al. High prevalence of bone disorders after gastrectomy. Am J Surg. 1997;174:431-438.

Downloaded from by Natalia Jara on May 19, 2011

136   Nutrition in Clinical Practice / Vol. 26, No. 2, April 2011

73. Bisballe S, Eriksen EF, Melsen F, Mosekilde L, Sorensen OH, Hessov I. Osteopenia and osteomalacia after gastrectomy: interrelations between biochemical markers of bone remodelling, vitamin D metabolites, and bone histomorphometry. Gut. 1991; 32:1303-1307. 74. Liedman B, Henningsson A, Mellstrom D, Lundell L. Changes in bone metabolism and body composition after total gastrectomy: results of a longitudinal study. Dig Dis Sci. 2000;45: 819-824. 75. Bernstein CN, Leslie WD. The pathophysiology of bone disease in gastrointestinal disease. Eur J Gastroenterol Hepatol. 2003;15: 857-864. 76. Ross AC, Manson JE, Abrams SA, et al. The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. J Clin Endocrinol Metab. 2011;96(1):53-58.

77. Copland L, Liedman B, Rothenberg E, Bosaeus I. Effects of nutrition support long time after total gastrectomy. Clin Nutr. 2007; 26:605-613. 78. Farahmand M, Sheppard BC, Deveney CW, Deveney KE, Crass RA. Long-term outcome of completion gastrectomy for nonmalignant disease. J Gastrointest Surg. 1997;1:182-187. 79. Tokunaga M, Hiki N, Ohyama S, et al. Effects of reconstruction methods on a patient’s quality of life after a proximal gastrectomy: subjective symptoms evaluation using questionnaire survey. Langenbecks Arch Surg. 2009;394:637-641. 80. Nunobe S, Okaro A, Sasako M, et al. Billroth 1 versus Roux-en-Y reconstructions: a quality-of-life survey at 5 years. Int J Clin Oncol. 2007;12:433-439. 81. Svedlund J, Sullivan M, Liedman B, Lundell L. Long term consequences of gastrectomy for patient’s quality of life: the impact of reconstructive techniques. Am J Gastroenterol. 1999;94:438-445.

Downloaded from by Natalia Jara on May 19, 2011

Nutricion gastrectomia