Postgastrectomy Syndromes

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GASTRIC SURGERY

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POSTGASTRECTOMY SYNDROMES J.

Chris Eagon, MO, Brent W. Miedema, MO, and Keith A. Kelly, MO

Postgastrectomy syndromes appear as constellations of signs and symptoms after gastric operations. The syndromes are brought about primarily by the changes in the motor function of the stomach and upper small intestine secondary to the operations and include dumping, small gastric remnant, postvagotomy diarrhea, chronic gastric atony, Roux stasis, alkaline reflux gastritis, and the afferent loop and efferent loop syndromes. The pathophysiology, diagnosis, and treatment of these syndromes form the basis of this report. Other long-term complications of gastric surgery, including recurrent ulcer, gastric remnant carcinoma, malabsorption, and anemia, are not as clearly related to disturbed gastric motility. They are not discussed here, nor are the acute complications of gastric surgery presented. INCIDENCE

Changes in the need for elective gastric surgery have led to a decrease in the frequency of postgastrectomy syndromes in recent years. For example, elective operations for peptic ulcer disease have declined nearly lO-fold over the last 30 years. 5, 22, 39, 53 This trend preceded Supported by US Public Health Service National Institutes of Health Grants DK07198 and DK18278 and the Mayo Foundation.

From the Departments of Surgery, Mayo Medical School, Rochester, Minnesota aCE and KAK) and University of Missouri, Columbia, Missouri (BWM)

SURGICAL CLINICS OF NORTH AMERICA VOLUME 72 • NUMBER 2 • APRIL 1992

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the introduction of H 2-receptor antagonists, although these drugs and the recently developed hydrogen pump antagonists have led to further decreases in elective surgical therapy. Newer gastric operations that minimally disturb gastric motor function, such as proximal gastric vagotomy (highly selective vagotomy, parietal-cell vagotomy), will likely also contribute to a continued decrease. A low rate of postgastrectomy syndromes follows proximal gastric vagotomy. This advantage offsets the disadvantage of a slightly higher incidence of ulcer recurrence after this operation compared with that which occurs after truncal vagotomy and antrectomy.33, 49, 66 While the need for elective operation for peptic ulcer has declined, the need for emergency surgery for this condition has remained steady over the last 20 years. 22, 53 Here, both the ulcer diathesis and its complications-bleeding, perforation, and obstruction-must be treated during the procedure. This sometimes means that more extensive antiulcer operations must be done, such as truncal vagotomy and subtotal gastrectomy. 44 The more extensive the gastric operation, the greater the incidence of postgastrectomy syndromes. When operations are done for peptic ulcer, postgastrectomy syndromes have been reported by from 5% to 50% of patients afterward, but in most reports, the incidence is near 20%.73 In a recent Japanese study of 535 patients, morbidity that prevented return to work within 6 months of operation occurred in 14% of patients after distal gastrectomy but in only 4% of patients after proximal gastric vagotomy.49 A prospective study by Donahue and associates documented a 26% incidence of long-term morbidity after truncal vagotomy and antrectomy versus only a 5% incidence with proximal gastric vagotomyY This difference underscores the physiologic significance of destruction or bypass of the pylorus and distal antrum in the development of the postgastrectomy syndromes. Another factor that influences the incidence of postgastrectomy syndromes is the sex of the patients: a female predominance is present. 74 The incidence may also vary depending on the definition of the syndrome used in a given study and on which syndromes are included. 32 PATHOGENESIS

Most postgastrectomy syndromes result from disturbances of gastric motility caused by the operation. To understand the pathogenesis, knowledge of the mechanisms that control gastric motility and emptying in health is helpful. Gastric Emptying in Health

The motor functions of the healthy stomach include a reservoir function to accept and store boluses of ingesta, a mechanical-digestive

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function to reduce large particles of food to a smaller size, and a transporting function to allow ingesta to pass into the small bowel for further digestion and absorption (Fig. 1). Initial decreases in the tone of the proximal stomach with swallowing (receptive relaxation) or with a large meal (accommodation) are vagally mediated responses that contribute in large part to the reservoir function of the stomach. Later, tonic contractions of the proximal stomach are important in transporting proximal gastric content toward the distal stomach and duodenum. Peristaltic contractions of the distal stomach and pylorus aide in the transport and mechanical trituration of large food particles. 46 Vagal stimulation of the distal stomach enhances these contractions. An intact pyloric region has a separating action that prevents the passage of large particles into the intestine 47 while controlling reflux of duodenal content into the stomach. The small bowel also has a role in gastric emptying by offering resistance to inflow from the stomach79 and by activating neural and hormonal mechanisms that provide feedback to the stomach to slow its emptying. Alterations after Operation

Gastric surgery may interfere with some or all of these gastric motor functions. Proximal gastric vagotomy impairs the compliance of Vagi: \

control tonic & phasic contractions

Pylorus:

controls emptying. ~ prevents reflux

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Duodenum: regulates emptying

Figure 1. Gastric anatomic elements and their roles in gastric emptying. Vagi, gastric nerves whose efferent fibers modulate proximal gastric tone (compliance) and strengthen gastric contractions. Proximal stomach large-volume reservoir that initially stores chyme and later propels it toward antrum. Distal stomach, low-volume, highly contractile segment that triturates solid food into particles <1 mm in diameter and propels chyme distally. Pylorus, thickening of circular muscle that prevents gastric emptying of large food particles and acts as a barricade to duodenal-gastric reflux. Duodenum, segment of small bowel that offers resistance to gastric outflow and, through neural and hormonal feedback mechanisms, diminishes gastric tone and increases pyloric contractions.

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the proximal stomach and decreases its reservoir function. Distal gastric vagotomy and distal gastric resection, including pyloric resection or ablation, decrease the mechanical-digestive function. The pyloric operations allow reflux of intestinal content back into the stomach. The type of gastroenterostomy may mechanically or functionally affect the transporting function of the stomach by either increasing or decreasing the resistance to outflow. Gastric mucosal functions that can be altered by gastric surgery include acid and enzymatic secretion, protection of the stomach from corrosive digestive juices, hormonal secretion that sustains the gastric phase of digestion, and secretion of intrinsic factor to facilitate vitamin B12 absorption. Alterations in these functions may contribute to the postgastrectomy syndromes. GENERAL APPROACH

Advances in the understanding of the control of gastric emptying have allowed the surgeon to categorize postgastrectomy syndromes more specifically. Anatomic factors that may relate to the syndrome need to be considered, and if possible, the exact type of the previous procedure should be determined. Usually, the modalities of endoscopy and barium radiography are needed. Scintigraphic imaging studies of gastric emptying using both liqilid- and solid-phase markers also are helpful to d.ocument the patterns of gastric emptying. In addition, the measurement of gastrointestinal motility, an excellent research tool, has sometimes proved of help in the management of patients. The postgastrectomy syndromes often improve with time. Except in severe cases, medical therapy should be attempted for at least 1 year (Table 1). Medical therapy consists primarily of dietary and behavioral modification. Psychological disturbances often accompany, and may exacerbate, the patient's symptoms, and a thorough attempt should be made to treat this component before offering surgical therapy. Should Table 1. MEDICAL AND SURGICAL TREATMENT OF THE POSTGASTRECTOMY SYNDROMES Specific Treatment Syndrome

Medical

Surgical*

Dumping Small gastric remnant Postvagotomy diarrhea Gastric atony Roux stasis Alkaline reflux Afferent loop Efferent loop

Diet modificationt Diet modificationt Diet modificationt Prokinetic drugs None Cholestyratnine None None

Roux-en-Y gastrojejunostomy Hunt-Lawrence jejunal pouch Antiperistaitic jejunal segment Near-total gastrectomy with Roux-en-Yt Near-totai gastrectomy with Roux-en-Yt Roux-en-Y gastrojejunostomyt Roux-en-Y gastrojejunostomyt Lysis of adhesionst

"The operative procedures listed are those preferred by the authors. tPtimary treatment modality.

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medical, dietary, and behavioral therapy fail, operation can be considered.

DUMPING SYNDROME

Dumping is one of the most common postgastrectomy syndromes. It can be separated into an early form and a late form based on the

interval between the ingestion of a meal and the onset of symptoms. Both forms are a response to the ingestion of hyperosmolar, carbohydrate-rich food. Early dumping begins within 10 to 30 minutes of meal ingestion and consists of both gastrointestinal and vasomotor symptoms. The gastrointestinal manifestations include fullness, crampy abdominal pain, nausea, vomiting, and explosive diarrhea. The vasomotor symptoms include diaphoresis, weakness, dizziness, flushing, and palpitations. Late dumping occurs 2 to 4 hours after a meal and consists of vasomotor symptoms similar to those present in early dumping, but gastrointestinal symptoms are absent. Because of the intense discomfort associated with meals, patients with dumping generally decrease their food intake. As a result, they lose weight and become malnourished.

Pathophysiology

The term "dumping" was coined by Mix in 1922 in reference to the rapid emptying of gastric content seen on barium radiography in patients with the condition. 50 The primary mechanisms leading to the dumping syndrome are loss of the reservoir function of the stomach and the rapid emptying of hyperosmolar carbohydrates into the small intestine. The four surgical factors that decrease reservoir function and speed gastric emptying are loss of proximal gastric receptive relaxation and accommodation with vagotomy, loss of gastric capacity with gastric resection, loss of the control of emptying with bypass or ablation of the pylorus, and loss of the duodenal feedback inhibition of gastric emptying with bypass of the duodenum by gastrojejunostomy. Experiments by Machella 40 and by Roberts and associates 62 demonstrated that the sudden appearance of large amounts of carbohydraterich liquid in the small intestine leads to fluid shifts from the intravascular space into the bowel lumen. This appears to be the primary factor producing the vasomotor and gastrointestinal symptoms of early dumping. In addition to the loss of intravascular volume, several enteric hormones, including serotonin,14 gastric inhibitory polypeptide (GIP), vasoactive inhibitory peptide (VIP),63 and neurotensin,68 are released during dumping and may be responsible for some of the vasomotor manifestations of early dumping. Late dumping is a result of the release of enteroglucagon in response to high carbohydrate concentrations in the small bowel. The enteroglucagon, in turn, sensitizes the f3-cell to

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stimuli and so causes hypersecretion of insulin. 67 After absorption of the carbohydrate is completed, the hyperinsulinemia causes hypoglycemia. Both the hypovolemia of early dumping and the hypoglycemia of late dumping are accompanied by the release of epinephrine, which contributes to the symptoms. The manifestations of early dumping are often made worse by ingestion of carbohydrates, whereas the symptoms of late dumping are relieved by their ingestion. The appearance of the dumping syndrome has been correlated with the rate of gastric emptying after truncal vagotomy and drainage 24 or truncal vagotomy and antrectomy.13 Those operative procedures, which cause rapid gastric emptying, are followed by a high incidence of dumping. The Billroth II gastrojejunostomy, which can result in extremely rapid emptying because it bypasses both the pyloric and the duodenal control mechanisms, is followed by an incidence of dumping in the early postoperative period that may exceed 50%. The Billroth I gastroduodenostomy and pyloroplasty retain duodenal resistance and have a lower incidence of dumping syndrome. In one series of 455 patients with truncal vagotomy and drainage, 14% developed dumping symptoms postoperatively.16 Because of the unique motility characteristics of the Roux limb in the Roux-en-Y gastrojejunostomy (see below), this type of anastomosis rarely results in gastric emptying rapid enough to produce dumping. Proximal gastric vagotomy can also speed gastric emptying. Vagal de nervation of the proximal stomach decreases receptive relaxation and accommodation,23 and this results in the more rapid emptying.48, 75, 78 This effect is relatively small, however; dumping after proximal gastric vagotomy occurs in only 1% to 6% of patients. 7, 20 Diagnosis

The diagnosis of dumping syndrome is made primarily on clinical grounds, but specific tests can be helpful. Scintigraphic studies using both solid- and liquid-phase markers can document rapid gastric emptying. In fact, normal gastric emptying precludes the diagnosis of dumping. Endoscopy and barium radiography are also helpful in precisely defining the anatomy and in aiding in the diagnosis of other postgastrectomy syndromes that may be present. Treatment

Dumping can generally be treated by medical means. Decreasing the size of meals, increasing the frequency of meals, taking liquids 30 minutes after meals, and avoiding concentrated carbohydrates are the mainstays of medical therapy. The synthetic somatostatin analogue octreotide has recently been used to treat dumping syndrome with some success. 58, 59 This action may be the result of the inhibitory effect of this substance on the release of enteric hormones. In approximately 1% of patients, however, severe symptoms of dumping will persist in spite of medical therapy, and operation will be required.

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Many different operations have been devised to treat dumping. Reconstruction of the pylorus after previous pyloroplasty led to improvement in dumping symptoms in eight of nine patients in one series,6 although only three of eight patients achieved good results in the Mayo Clinic experienceY Conversion of a gastrojejunostomy to a gastroduodenostomy re-establishes the normal gastroduodenal flow and allows duodenal receptors to mediate slowing of gastric emptying. At Mayo, of five patients undergoing this procedure, three obtained good or excellent resultsY Interposition of a lO-cm jejunal segment in either the isoperistaltic or the antiperistaltic position has been recommended. During the 1970s at the Mayo Clinic, of 31 patients operated on for dumping, 13 underwent this interposition operation. Of these, three achieved excellent and six achieved good results. 37 The Roux-en- Y gastrojejunostomy is emerging as an excellent operation for the dumping syndrome (Fig. 2). This operation has been used successfully by several groups of surgeons. 37, 77, 81 Animal and human studies of the motor function of the Roux limb have elucidated the mechanism by which this operation causes slowed gastric emptying. Transection of the jejunum during construction of the limb results in a decrease in the frequency of contractions in the limb,60 and, at least in the dog, many of these contractions originate from ectopic pacemakers in the mid portion of the limb that drive the proximal portion of the limb backward. 36 These retrograde contractions increase the resistance to the transit of chyme through the limb and slow gastric emptying. 34 In a series of 22 patients who underwent the Roux procedure for the dumping syndrome, 17 had resolution of dumping symptoms. 77 However, five patients developed gastric stasis after the procedure.

Figure 2. Roux-en-Y gastrojejunostomy, The jejunum is transected 20 cm distal to the ligament of Treitz. The distal cut end is closed, and the gastric remnant is anastomosed to it in an endto-side, isoperistaltic fashion just distal to the closure. The proximal cut end of jejunum is anastomosed in an end-to-side fashion to the mid jejunum 40 cm distal to the gastrojejunostomy.

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SMALL GASTRIC REMNANT SYNDROME

The small gastric remnant syndrome, also called the "early satiety syndrome," is related to the loss of the reservoir function of the stomach and is most prevalent after operations that remove 80% or more of the stomach. lO The symptoms include early satiety, epigastric pain soon after starting a meal, and vomiting. Usually the symptoms are mild, but occasionally, severe weight loss, malnutrition, and anemia attributable to folate, vitamin B12, or iron deficiency result. Pathophysiology and Diagnosis

Similar to the dumping syndrome, the mechanism responsible for the small remnant syndrome is the loss of the reservoir function of the stomach. However, rapid gastric emptying is not a primary feature. Surgical factors that reduce the gastric reservoir function include loss of receptive relaxation and accommodation with vagotomy and a decrease in capacity with gastric resection. The diagnosis is based mostly on the clinical history. Treatment

Medical management of this syndrome is generally successful. Increasing the frequency and decreasing the size of meals and adding supplemental vitamins, iron, and pancreatic enzymes ameliorate symptoms. Complicated operations involving construction of a pouch have been devised for the rare patient with intractable postprandial pain and weight loss. For patients with a Billroth II anastomosis, the HuntLawrence pouch30 or the Tanner Roux-19 pouch72 may be utilized. 26 Both these procedures involve transection of the afferent jejunal limb and creation of a Roux-en-Y gastrojejunostomy. In the Hunt-Lawrence pouch, the afferent limb is anastomosed side-to-side to the efferent limb, making a proximal pouch. In the Tanner Roux-19 procedure, the distal cut end of the afferent limb is anastomosed to the Roux limb, making a loop reservoir. The complications of stasis and ulceration with these reconstructive procedures mandate that they be used only in patients with severe symptoms unresponsive to other therapies. POSTVAGOTOMY DIARRHEA

All types of gastric surgery may result in diarrhea postoperatively, but the incidence of diarrhea is higher in patients who have undergone vagotomy. Truncal vagotomy has the highest incidence, around 20%,71 whereas the incidences with selective vagotomy and pyloroplasty and proximal gastric vagotomy are 6% and 4%, respectivelyY Diarrhea is

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usually episodic. Attacks of explosive diarrhea may last several days and then may not recur for several months. Symptoms of dumping may also be present, but postvagotomy diarrhea can usually be distinguished from the diarrhea associated with dumping episodes. Symptoms generally improve over the first year after operation and rarely remain a severe and constant problem. Pathophysiology

The underlying mechanism of postvagotomy diarrhea is unclear. The progressively decreasing incidence with more selective vagotomies implicates vagal denervation of the small bowel or biliary tree in the pathogenesis. Also, changes in the rate of gastric emptying have been implicated. Decreased receptive relaxation and rapid liquid gastric emptying have been correlated with the presence of postvagotomy diarrhea. 23, 54 Changes in the rate and pathway of the enteric flow of chyme may lead to relative malabsorption of nutrients normally digested by mucosal enzymes. In this manner, for example, subclinical lactase deficiency may be unmasked by gastric surgery and result in postoperative diarrhea in response to foods that formerly did not cause symptoms. . Diagnosis

No specific tests are available. The diagnosis is made on clinical grounds, with care taken to distinguish other postgastrectomy syndromes that often occur concomitantly. Other causes of diarrhea should be considered as well. Routine stool culture and measurement of fecal fat output should be undertaken. Gluten-sensitive enteropathy may occur after gastrectomy and can present as diarrhea and malabsorption. In patients with weight loss and malabsorption, endoscopy with smallbowel biopsy should be performed. Treatment

Dietary measures that are effective include decreasing the intake of both fluid and lactose-containing foods. Antidiarrheal agents such as diphenoxylate with atropine or loperamide71 and the bile salt exchange resin cholestyramine 1 are also useful. Surgical therapy is rarely recommended, but when it is, a 10- to IS-cm antiperistaltic jejunal segment constructed 100 cm distal to a gastroenterostomy or to the ligament of Treitz has been used with some success. 8 In one series of 19 patients with severe postvagotomy diarrhea, 68% of patients achieved an excellent result and 21 % achieved a good result with this procedure. 65

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CHRONIC GASTRIC ATONY

A decrease in gastric motor tone can result from gastric surgery and can cause delayed gastric emptying. These patients complain of epigastric fullness and pain, nausea after eating, and vomiting of partially digested food eaten hours or even days before. Many patients cannot tolerate solids but can maintain adequate nutrition on liquids. The symptoms can become so severe that malnutrition and weight loss occur even on a liquid diet. The clinical picture may be complicated further by bezoar formation, which occurs in as many as 12% of patients with the condition. 19 Pathophysiology

Gastric atony results primarily from the loss of gastric vagal innervation. The tonic contractions of the proximal stomach in the late stages of gastric emptying are under vagal control. Indeed, denervation of the proximal stomach by proximal gastric vagotomy can result in gastric atony in 0.7%31,33 to 3%29 of patients. Strong peristaltic antral contractions in the postprandial period are also controlled by the vagi. The loss of these contractions inhibits the mechanical-digestive function of the stomach. Less selective vagotomies have a higher incidence of delayed gastric emptying. 29 In the Mayo Clinic experience during the 1970s, of the 15 patients requiring reoperation for gastric stasis, 12 had had a truncal vagotomy as part of the original procedure. 37 Underlying conditions that increase the risk of developing gastric atony include preoperative gastric outlet obstruction,38, 80 diabetes mellitus, hypothyroidism, and autonomic neurologic disorders. Diagnosis

The most important issue in the differential diagnosis of this syndrome is determining whether the impedance to gastric outflow is mechanical or functional. Contrast radiography usually demonstrates a distended, flaccid gastric remnant without evidence of mechanical obstruction. Endoscopy confirms the absence of an obstructing gastroenterostomy. The diagnosis is confirmed using scintigraphic imaging, which shows delayed gastric emptying, especially of solids. Treatment

Medical therapy with prokinetic agents, such as metoclopramide and erythromycin, has had limited success,15 and many patients require revisional surgery. Because vagal innervation cannot be restored, operative therapy is aimed at decreasing the reservoir capacity of the

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stomach. In the case of previous vagotomy and pyloroplasty, an antrectomy can be attempted. More often, the gastric remnant is so massively distended, atonic, and flaccid that a near-total gastric resection is required. To prevent the development of bile reflux esophagitis, the Roux-en-Y gastrojejunostomy should be used in conjunction with near-total gastrectomy55 (Fig. 3). In the Mayo Clinic experience, among 40 patients with chronic gastric atony who underwent extensive distal gastric resection and Roux-en-Y gastrojejunostomy, 23 achieved excellent or good postoperative results, 4 had fair results, and 13 did not improve. 35 A similar success rate occurred in another group of 15 patients with postsurgical gastroparesis; 13 of them reported satisfactory results after near-total Roux gastrectomy. 15 ROUX STASIS SYNDROME

Patients with the Roux-en-Y gastroenterostomy are at increased risk for delayed gastric emptying and the symptoms of epigastric fullness, abdominal pain, nausea, and food vomiting. Severe symptoms can lead to malnutrition and weight loss. Gastric bezoars may develop. The prevalence of the syndrome ranges from 10% to 50% in patients at risk. 3, 27 In a large retrospective review from the Mayo Clinic, 30% of 202 patients who had had a Roux gastrojejunostomy developed signs and symptoms of Roux stasis syndrome. 21 Pathophysiology

Although the relative contributions to stasis are not entirely clear, both the vagotomized gastric remnant and the Roux limb have roles in development of the Roux stasis syndrome. As with gastric atony,

~20cm Figure 3. Near-total gastrectomy with Roux-enY gastrojejunostomy, Removal of almost all of the gastric remnant decreases the symptoms of stasis in patients with chronic gastriC atony. Reflux esophagitis is rare with this procedure.

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vagotomy decreases the tone of the gastric remnant, and removal of the atonic stomach often leads to improvement in symptoms. 15, 21 This does not completely explain the syndrome, however, because Roux stasis syndrome can also be present after total gastrectomy and esophagojejunostomy. In the Mayo Clinic study of Roux-Y gastrectomy, 2 of 32 patients with total gastrectomy and Roux esophagojejunostomy developed symptoms of Roux stasis.21 Transit through the Roux limb itself has been measured scintigraphically and found to be slowed. 57 The length of the Roux limb has been correlated with an increased incidence of Roux stasis syndrome. 21 Recent studies of the motor patterns of the Roux limb have elucidated the mechanism of delayed transit through this intestinal segment. Normally, the mechanical contractions of the jejunum are controlled by electrical depolarizations of the smooth musculature, called pacesetter potentials, which propagate from the duodenum distally down the jejunum. 25 Transection of the jejunum in the construction of the Roux limb prevents this propagation and results in a lower frequency of pacesetter potentials in the limb. 60 Electrical and motility measurements in the dog have shown that ectopic pacemakers develop within the limb. These pacemakers generate pacesetter potentials, which, with their associated contractions, move toward the stomach. 36 This results in slower transit through the limb. 34 In addition to the retrograde propagation of pacesetter potentials, both human and animal studies have shown that phase III of the interdigestive motor complex occurs more frequently in the Roux limb than in the healthy jejunum. Phase III is a cyclically recurring pattern of organized intense motor activity during the fasting state that is thought to be important in sweeping the bowel clear of residual content after digestion is complete. The phase Ills that occur in the Roux limb, however, are irregular and do not propagate distally as well as they do in health. 18, 42 This abnormal pattern in the Roux limb may mean that the limb is not swept as clean as the jejunum in health. Finally, truncal vagotomy results in loss of vagal innervation to the jejunum. This may diminish the strength of jejunal contractions.

Diagnosis

As with gastric atony, it is important to rule out mechanical causes of obstruction when evaluating patients with possible Roux stasis. Barium radiography and endoscopy are useful here. Scintigraphic imaging is the best method to quantitate the delayed emptying of solids and liquids through the gastric remnant and Roux limb. Although emptying studies are helpful, the treatment will be determined by the severity of symptoms and not by the specific results of gastric emptying studies.

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Treatment

Medical therapy for Roux stasis syndrome is seldom successful, and revisional surgery is often required. Surgical therapy usually includes a near-total gastrectomy and adjustment of the length of the Roux limb to a final length of 40 cm. In one series of 18 patients with daily vomiting after Roux gastrectomy, extensive gastric resection resulted in symptomatic improvement and weight gain in 15 patients. 28 This procedure is not entirely satisfactory, however. Persistence of Roux stasis syndrome is the major negative outcome. No current method is available to reverse the motor abnormalities in the Roux limb once the limb has been constructed. ALKALINE REFLUX GASTRITIS

Five to fifteen percent of patients undergoing gastric surgery develop symptoms of alkaline reflux gastritis/o including burning epigastric pain, nausea, and bilious vomiting that does not relieve the abdominal pain. The onset of pain usually is not associated with meals, although meals may exacerbate the pain. The vomitus often contains food mixed with the bile. These symptoms result in diminished caloric intake, weight loss, and anemia. Alkaline reflux gastritis requires surgical treatment more often than any other postgastrectomy syndrome. 61 Of 173 patients undergoing reconstructive gastric surgery at Mayo Clinic over a la-year period, 125 had enterogastric reflux as the main problem. 37 Pathophysiology

Reflux gastritis results when the pylorus is resected, bypassed, or destroyed, allowing intestinal content to reflux into the stomach. For this syndrome to develop, the anastomosis must allow the stream of bilious intestinal content to contact the gastric mucosa. The Billroth II gastrojejunostomy has the highest incidence of this disorder; loop gastrojejunostomy, Billroth I, and pyloroplasty have lesser incidences. 10 Which component of intestinal fluid is the injurious one is not clear, but bile salts are thought to be involved. In a prospective histologic study of 17 patients, bilious reflux was more common after Billroth II operations than after Roux-Y gastrojejunostomy. 52 The severity of reflux, however, does not correlate with the presence of symptoms. Delayed clearance of bile is also thought to be important in the pathogenesis of this syndrome. 41 Diagnosis

Endoscopic examination with gastric mucosal biopsy and examination of the gastric anastomosis should be performed to make the

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diagnosis and to rule out afferent loop syndrome, the principal differential diagnosis in patients with bilious vomiting. The endoscopist sees bile refluxing into the stomach, which is lined by an acutely inflamed, even ulcerated, mucosa. Mucosal biopsies will show intestinalization of the gastric glands, inflammation, ulceration, and hemorrhage, although the severity of the symptoms does not correlate with the histologic changes. Some surgeons recommend evaluation of gastric emptying with scintigraphic imaging before planning revisional surgery, because delayed bile clearance may be involved and because the most frequent complication of surgical treatment is delayed gastric emptying. 10 Scintigraphic assessment of the magnitude of reflux can be done by tagging bile with a radioactive marker and determining the percentage of the secreted isotope refluxed into the stomach. Treatment

Medical treatment is generally ineffective. Agents that bind bile salts, such as cholestyramine, although theoretically attractive, have not worked in clinical practice. 45 The operative therapy most often utilized is the Roux-en-Y gastrojejunostomy, which diverts pancreaticobiliary secretions away from the gastric remnant. Of 92 patients with enterogastric reflux treated with the Roux procedure at our institution, 75% had an excellent or good result. 37 If vagotomy was not performed at the primary operation, it should be performed at the time of the Roux procedure to prevent development of a stomal ulcer in the proximal Roux limb. Because of the high incidence of postoperative Roux stasis syndrome and because development of Roux stasis syndrome cannot be predicted from preoperative gastric emptying studies,56 some surgeons recommend adding subtotal gastrectomy to the Roux procedure to speed gastric emptying in the postoperative period. The Henley jejunal interposition has also been used to treat alkaline reflux gastritis. Bile reflux after the Henley procedure, just as after the Roux procedure, measures less than 1 % of secreted isotope, whereas ulcer patients who have not been operated on and patients with a Billroth II anastomosis had 2.5% and 32% reflux, respectively.69 We have little experience with the Henley procedure. The recently described ""duodenal switch" procedure can also be used in those rare patients in whom alkaline reflux gastritis occurs through an intact pylorus. 11 In this procedure, the duodenum is transected 5 to 7 cm distal to the pylorus, the distal cut end is closed, and the proximal duodenal cut end is anastomosed end-to-end to a jejunal Roux limb. Early experience has shown symptomatic and endoscopic improvement in 9 of 10 patients. THE LOOP SYNDROMES Afferent Loop Syndrome

Afferent loop syndrome results from obstruction of the afferent limb of a loop gastrojejunostomy. It occurs in both an acute and a

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chronic form. The acute form usually appears within the first 1 to 2 weeks after operation, although it may appear as long as 30 years after gastrectomyY The condition results from complete obstruction of the afferent limb secondary to a kink, herniation, or volvulus. Because of the better recognition of the anatomic factors causing this syndrome, including the use of a long afferent limb, it is now quite rare. 26 Patients may complain of severe abdominal pain, nausea, and vomiting without bile. A fluid-filled mass may be apparent on physical or radiographic examination or on ultrasound studiesY As pressure in the afferent limb increases, the serum amylase concentration may rise, duodenal stump leakage may occur, and pressure necrosis may develop in the limb. Immediate operative therapy is necessary. At operation, a jejunojejunostomy is done provided pressure necrosis of the afferent limb has not occurred. More extensive resections including a pancreaticoduodenectomy may be required when ischemic injury is severe. The chronic form of the afferent loop syndrome is a result of chronic partial obstruction of the afferent limb. The symptoms include right upper-quadrant pain brought on by meals, nausea, and bilious vomiting, which is usually not mixed with food and which relieves the abdominal pain. The patient will limit food intake to minimize the symptoms. Weight loss results. Furthermore, the stasis in the obstructed loop allows a "blind loop" syndrome to occur, with bacterial overgrowth, bile salt deconjugation, steatorrhea, and vitamin B12 and iron deficiency. Chronic afferent loop syndrome may be caused by several mechanisms. As in the acute form, kinking or herniation of a redundant afferent limb may result in partial obstruction. In the chronic form, anastomotic stricture, adhesion formation, stomal ulceration, jejunogastric intussusception, and carcinoma may be responsible. Sudden release of bile into the gastric remnant after food has already emptied from the stomach results in bilious vomiting and relief of pain. The principal diagnostic challenge is to separate alkaline reflux gastritis from this disorder. Endoscopy is the modality of choice. The anastomotic site can be examined under direct vision and pathologic lesions identified and biopsied as warranted. Once the diagnosis is made, surgical correction is indicated. The Billroth II anastomosis may be revised to a Billroth I. Construction of a Roux-en-Y gastrojejunostomy may be simpler and has been met with good clinical results. 4

Efferent Loop Syndrome

The efferent loop syndrome is related to partial or complete mechanical obstruction of the efferent limb at or near the gastrojejunostomy. Symptoms, which may occur months to years after the operation, consist of diffuse abdominal pain, nausea, and bilious vomiting. When symptoms present in the chronic form, the obstruction

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is partial and often intermittent. The diagnosis is confirmed by contrast radiography, which demonstrates slow or absent gastric emptying across a point of obstruction in the efferent limb. Operative therapy is required. At laparotomy, a common cause is found to be an adhesive band obstructing the efferent limb near the gastric anastomosis. 26 Other possible causes include retroanastomotic herniation of the efferent limb through unclosed defects in the mesocolon or abdominal parietes, jejunogastric intussusception, stomal ulcer, and gastric carcinoma. The operative procedure may consist only of lysis of adhesions. However, other operative findings may dictate the need for revision of the anastomosis or conversion to a Billroth I or Roux-en-Y gastrojejunostomy. FUTURE TRENDS

Recent canine studies of gastrointestinal pacing have shown that this technique may have application in the treatment of the dumping syndrome. The slowing of gastric emptying with the Roux procedure can be enhanced by retrograde pacing of the Roux limb. Such pacing slows emptying by enhancing contractions in the limb which move toward the stomach. 9 The hypovolemia seen in dumping can be decreased in dogs with retrograde pacing of the duodenum. 2 Other studies have shown that retrograde gastric pacing also slows gastric emptying.64 Future clinical application of these techniques may result in more effective and less morbid treatment for the dumping syndrome. Intestinal pacing may also have a role in the Roux stasis syndrome. Pacing the Roux limb in a forward direction in dogs speeds transit of both liquids and solids through the limb after vagotomy and Roux gastrectomy.34 Thus far, however, pacing of the human jejunum has not been consistently successful. 60 A new operative therapy has emerged recently that may be useful in preventing the Roux stasis syndrome. This operation is called the "uncut Roux" gastroenterostomy.76 Here, a loop gastrojejunostomy is made, the afferent limb of which is occluded by staples. The staples prevent flow of content across the staple line but allow normal propagation of intestinal pacesetter potentials to the Roux limb. Proximal to the staple line, the afferent loop and efferent loop of the gastrojejunostomy are anastomosed in a side-to-side fashion (Fig. 4). With respect to the flow of bile, this procedure functions like a Roux procedure, but the adverse effects of jejunal transection are avoided. At this point, the problem of dehiscence of the staple line in the postoperative period has not been solved. 51 Nonetheless, the uncut Roux may prove to be a useful construction in the future. SUMMARY

Anatomic and physiological changes introduced by gastric surgery result in postgastrectomy syndromes in approximately 20% of patients.

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staple line

Figure 4. "Uncut" Roux gastrojejunostomy. The staple line prevents flow of enteric content toward the stomach but permits transmission of pacesetter potentials, hence coordinated contractions, to the Roux limb.

. . . Bilious enteric stream Jejunal pacesetter potential propagation . . . Gastric enteric stream

Most of these disorders are caused by operation-induced abnormalities in the motor functions of the stomach, including disturbances in the gastric reservoir function, the mechanical-digestive function, and the transporting function. Division of the vagal innervation to the stomach and ablation or bypass of the pylorus are the most significant factors contributing to postgastrectomy syndromes. Either rapid or slow emptying may result, depending on the relative importance of lack of a compliant gastric reservoir, loss of an effective contractile force, and loss of controlling factors that slow or speed gastric emptying and result in duodenal-gastric reflux. Clearly defining which syndrome is present in a given patient is critical to developing a rational treatment plan. In syndromes with slow gastric emptying, bilious vomiting, or alkaline reflux gastritis, the use of endoscopy is essential to rule out mechanical causes of the syndrome. Contrast radiography and scintigraphic gastric emptying studies are useful to document rapid or delayed gastric emptying. Postgastrectomy syndromes often abate with time. Conservative measures, including medical, dietary, and behavioral therapy, should be given at least a 1-year trial. If these nonoperative measures fail, surgical therapy is recommended. The Roux-en-Y gastrojejunostomy is useful for patients with dumping, because it slows gastric emptying and the transit of chyme through the Roux limb. The same operation helps patients with alkaline reflux gastritis, because it diverts pancreaticobiliary secretions away from the gastric remnant. Near-total gastrectomy, which reduces the size of a flaccid gastric reservoir, can be used to treat delayed gastric emptying. This operation should be combined with the Roux procedure to prevent postoperative reflux gastritis and esophagitis. Newer techniques, such as gastrointestinal

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pacing and the uncut Roux operation, may improve the treatment of the postgastrectomy syndromes in the future. References 1. Allan JG, Russell RI: Cholestyramine in treatment of postvagotomy diarrhoeadouble-blind controlled trial. Br Med J 1:674-676, 1977 2. Becker JM, Sava P, Kelly KA, et al: Intestinal pacing for canine postgastrectomy dumping. Gastroenterology 84:383-387, 1983 3. Britten JP, Johnston 0, Ward De, et al: Gastric emptying and clinical outcome after Roux-en-Y diversion. Br J Surg 74:900-904, 1987 4. Brook-Cowden GL, Braasch JW, Gibb SP, et al: Postgastrectomy syndromes. Am J Surg 131:464-470, 1976 5. Burkhalter E: Incidence of gastrectomy in United States Army hospitals worldwide from 1975 to 1985. Am J Gastroenterol 83:1231-1234, 1988 6. Cheadle WG, Baker PR, Cuschieri A: Pyloric reconstruction for severe vasomotor dumping after vagotomy and pyloroplasty. Ann Surg 202:568-572, 1985 7. Clarke RJ, Alexander-Williams J: The effect of preserving antral innervation and of a pyloroplasty on gastric emptying after vagotomy in man. Gut 14:300-307, 1973 8. Craft IL, Venables CW: Antiperistaltic segment of jejunum for persistent diarrhea following vagotomy. Ann Surg 167:282-286, 1968 9. Cranley B, Kelly KA, Go VLW, et al: Enhancing the anti-dumping effect of Roux gastrojejunostomy with intestinal pacing. Ann Surg 198:516-524, 1983 10. Delcore R, Cheung LY: Surgical options in postgastrectomy syndromes. Surg Clin North Am 71:57-75, 1991 11. Demeester TR, Fuchs KH, Ball CS, et al: Experimental and clinical results with proximal end-to-end duodenojejunostomy for pathologic duodenogastric reflux. Ann Surg 206:414-426, 1987 12. Donahue PE, Bombeck CT, Condon RE, et al: Proximal gastric vagotomy versus selective vagotomy with antrectomy: Results of a prospective randq,mized clinical trial after four to twelve years. Surgery 96:585-590, 1984 13. Donovan lA, Gunn IF, Brown A, et al: A comparison of gastric emptying before and after vagotomy with antrectomy and vagotomy with pyloroplasty. Surgery 76:729732, 1974 14. Drapanas T, McDonald lC, Stewart JD: Serotonin release following instillation of hypertonic glucose into the proximal intestine. Ann Surg 156:528-536, 1962 15. Eckhauser FE, Knol JA, Raper SA, et al: Completion gastrectomy for postsurgical gastroparesis syndrome: Preliminary results with 15 patients. Ann Surg 208:345-353, 1988 16. Eisenberg MM, Woodward ER, Carson TJ: Vagotomy and drainage procedure for duodenal ulcer: The results of ten years' experience. Ann Surg 170:317-328, 1969 17. Emas 5, Fernstrom M: Prospective randomized trial of selective vagotomy with pyloroplasty and selective proximal vagotomy with or without pyloroplasty in the treatment of duodenal, pyloric, and prepyloric ulcers. Am J Surg 149:236-243, 1985 18. Fich A, Neri M, Camilleri M, et al: Stasis syndromes following gastric surgery: Clinical and motility features of 60 symptomatic patients. J Clin Gastroenterol 12:505512, 1990 19. Goldstein HM, Cohen LE, Hagen RO, et al: Gastric bezoars: A frequent complication in the postoperative ulcer patient. Radiology 107:341-344, 1973 20. Goligher Je, Hill GL, Kenney TE, et al: Proximal gastric vagotomy without drainage for duodenal ulcer: Results after 5-8 years. Br J Surg 65:145-51, 1978 21. Gustavsson 5, Ilstrup OM, Morrison P, et al: Roux-Y stasis syndrome after gastrectomy. Am J Surg 155:490-494, 1988 22. Gustavsson 5, Kelly KA, Melton LJ, et al: Trends in peptic ulcer surgery: A population based study in Rochester, Minnesota, 1956-1985. Gastroenterology 96:688-696, 1988 23. Hartley MN, Mackie CR: Gastric adaptive relaxation and symptoms after vagotomy. Br J Surg 78:24-27, 1991

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24. Haynes 5, Thomson JPS, Brown N, et al: A study of the relationship between the rate of gastric emptying and the dumping syndrome [abstract]. Br J Surg 60:307-308, 1973 25. Hermon-Taylor J, Code CF: Localization of the duodenal pacemaker and its role in the organization of duodenal myoelectric activity. Gut 12:40-47, 1971 26. Herrington JL Jr, Sawyers JL: Complications following gastric operations. In Schwartz 51, Ellis H (eds): Maingot's Abdominal Operations, ed 9. Norwalk, Connecticut, Appleton & Lange, 1989, pp 701-730 27. Herrington JL, Scott HW, Sawyers JL: Experience with vagotomy-antrectomy and Roux-en-Y gastrojejunostomy in surgical treatment of duodenal, gastric, and stomal ulcers. Ann Surg 199:590-597, 1984 28. Hinder RA, Esser J, DeMeester TR: Management of gastric emptying disorders following the Roux-en-Y procedure. Surgery 104:765-772, 1988 29. Hom 5, Sarr MG, Kelly KA, et al: Postoperative gastric atony after vagotomy for obstructing peptic ulcer. Am J Surg 157:282-286, 1989 30. Hunt q, Cope JS: Modified technic for total gastrectomy with formation of a food pouch from the jejunum. Am Surg 18:85-90, 1952 31. Johnston 0: Operative mortality and postoperative morbidity of highly selective vagotomy [abstract]. Br J Surg 62:160, 1975 32. Johnston 0, Blackett RL: A new look at selective vagotomies. Am J Surg 156:416427, 1988 33. Johnston GW, Spencer EFA, Wilkinson AJ, et al: Proximal gastric vagotomy: Follow up at 10-20 years. Br J Surg 78:20-23, 1991 34. Karlstrom L, Kelly KA: Ectopic jejunal pacemakers and gastric emptying after Roux gastrectomy: Effect of intestinal pacing. Surgery 106:867-871, 1989 35. Karlstrom L, Kelly KA: Roux gastrectomy for chronic gastric atony. Am J Surg 157:4449, 1989 36. Karlstrom L, Soper NJ, Kelly KA, et al: Ectopic jejunal pacemakers and enterogastric reflux after Roux gastrectomy: Effect of intestinal pacing. Surgery 106:486-495, 1989 37. Kelly KA, Becker JM, van Heerden JA: Reconstructive gastric surgery. Br J Surg 68:687-691, 1981 38. Kraft RO, Fry WJ, DeWeese MS: Postvagotomy gastric atony. Arch Surg 88:865, 1964 39. Kurata JH, Corboy ED: Current peptic ulcer time trends: An epidemiological profile. J Clin Gastroenterol 10:259-268, 1988 40. Machella TE: The mechanism of the post-gastrectomy "dumping" syndrome. Ann Surg 130:145-159, 1949 41. Mackie C, Hulks G, Cuschieri A: Enterogastric reflux and gastric clearance of refluxate in normal subjects and in patients with and without bile vomiting following peptic ulcer surgery. Ann Surg 204:537-542, 1986 42. Mathias JR, Fernandez A, Sninsky CA, et al: Nausea, vomiting and abdominal pain after Roux-en-Y anastomosis: Motility of the jejunal limb. Gastroenterology 88:101107, 1985 43. Matsusue 5, Kashihara 5, Takeda H, et al: Three cases of afferent loop obstruction: The role of ultrasonography in the diagnosis. Jpn J Surg 18:709-713, 1988 44. McConnel DB, Baba Gc, Deveney CW: Changes in surgical treatment of peptic ulcer disease within a Veterans Hospital in the 1970's and the 1980's. Arch Surg 124:11641167, 1989 45. Meshkinpour H, Elashoff J, Stewart H, et al: Effect of cholestyramine on the symptoms of reflux gastritis. Gastroenterology 73:441-443, 1977 46. Meyer JH: Motility of the stomach and gastroduodenal junction. In Johnson LR (ed): Physiology of the Gastrointestinal Tract, ed 2. New York, Raven Press, 1987, pp 613629 47. Meyer JH, Thompson JB, Cohen MB, et al: Sieving of solid food by the canine stomach and sieving after gastric surgery. Gastroenterology 76:804-813, 1979 48. Mistiaen W, Van Hee R, Block P, et al: Gastric emptying for solids in patients with duodenal ulcer before and after highly selective vagotomy. Dig Dis Sci 35:310-316, 1990 49. Misumi A, Harada K, Murakami A, et al: Postoperative results of distal partial gastrectomy, selective vagotomy plus antrectomy, and selective proximal vagotomy for duodenal ulcers. Jpn J Surg 19:708-717, 1989

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50. Mix CL: "Dumping stomach" following gastrojejunostomy. Surg Clin North Am 2:617-622, 1922 51. Mulholland MW, Magellanes F, Quigley TM, et al: In-continuity gastrointestinal stapling. Dis Colon Rectum 26:586-589, 1983 52. Offerhaus GJA, Rieu PNMA, Jansen JBMJ, et al: Prospective comparative study of the influence of postoperative bile reflux on gastric mucosal histology and Campylobacter pylori infection. Gut 30:1552-1557, 1989 53. Paimela H, Tuompo PK, Perakyla T, et al: Peptic ulcer surgery during the H,-receptor antagonist era: A population-based epidemiological study of ulcer surgery in Helsinki from 1972 to 1987. Br J Surg 78:28-31, 1991 54. Parr NJ, Grime S, Brownless S, et al: Relationship between gastric emptying of liquid and postvagotomy diarrhoea. Br J Surg 75:279-282, 1988 55. Payne WS: Prevention and treatment of biliary-pancreatic reflux esophagitis: The role of long-limb Roux-Y. Surg Clin North Am 63:851-858, 1983 56. Pellegrini CA, Patti MG, Lewin M, et al: Alkaline reflux gastritis and the effect of biliary diversion on gastric emptying of solid food. Am J Surg 150:166-171, 1985 57. Perino LE, Adcock KA, Goff JS: Gastrointestinal symptoms, motility, and transit after Roux-en-Y operation. Am J Gastroenterol 83:380-385, 1988 58. Primrose IN, Johnston 0: Somatostatin analogue SMS 201-995 (octreotide) as a possible solution to the dumping syndrome after gastrectomy or vagotomy. Br J Surg 76:140-144, 1989 59. Reasbeck PG, Van Rij AM: The effect of somatostatin on dumping after gastric surgery: A preliminary report. Surgery 99:462-468, 1986 60. Richter HM III, Kelly KA: Effect of transection and pacing on human jejunal pacesetter potentials. Gastroenterology 91:1380-1385, 1986 61. Ritchie WP Jr: Alkaline reflux gastritis: An objective assessment of its diagnosis and treatment. Ann Surg 192:288-298, 1980 62. Roberts KE, Randall HT, Farr HW, et al: Cardiovascular and blood volume alterations resulting from intrajejunal administration of hypertonic solutions to gastrectomized patients: The relationship of these changes to the dumping syndrome. Ann Surg 140:631-640, 1954 63. Sagor GR, Bryant MG, Ghatei MA, et al: Release of vasoactive intestinal peptide in the dumping syndrome. Br Med J 282:507-510, 1981 64. Sarna SK, Bowes KL, Daniel EE: Gastric pacemakers. Gastroenterology 70:226-231, 1976 65. Sawyers JL: Management of postgastrectomy syndromes. Am J Surg 159:8-14, 1990 66. Schirmer BD: Current status of proximal gastric vagotomy. Ann Surg 209:131-148, 1989 67. Shultz KT, Neelon FA, Nilsen LB, et al: Mechanism of postgastrectomy hypoglycemia. Arch Intern Med 128:240-246, 1971 68. Sirinek KR, O'Dorisio TM, Howe B, et al: Neurotensin, vasoactive intestinal peptide, and Roux-en-Y gastrojejunostomy: Their role in the dumping syndrome. Arch Surg 120:605-609, 1985 69. Sousa JES, Troncon LEA, Andrade JI, et al: Comparison between Henley jejunal interposition and Roux-en-Y anastomosis as concerns enterogastric biliary reflux levels. Ann Surg 208:597-599, 1988 70. Stabile BE, Passaro E Jr: Sequelae of surgery for peptic ulcer. In Berk JE (ed): Bockus Gastroenterology, ed 4. Philadelphia, WB Saunders, 1985, pp 1225-1254 71. Storer EH: Postvagotomy diarrhea. Surg Clin North Am 56:1461-1468, 1976 72. Tanner NC: Personal observations and experiences in the diagnosis and management of ulcer disease and disabilities that follow peptic ulcer operations. Surg Clin North Am 56:1349-1363, 1976 73. Thompson Je, Weiner T: Evaluation of surgical treatment of duodenal ulcer: Shortand long-term effects. Clin Gastroenterol 13:569-600, 1984 74. Tovey FI, Godfrey JE, Lewin MR: A gastrectomy population: 25-30 years on. Postgrad Med J 66:450-456, 1990 75. Van Hee R, Mistiaen W, Block P: Gastric emptying of liquids after highly selective vagotomy for duodenal ulcer. Hepatogastroenterology 36:92-96, 1989 76. Van Stiegmann G, Goff JS: An alternative to Roux-en-Y for treatment of bile reflux gastritis. Surg Gynecol Obstet 166:69-70, 1988

POSTGASTRECTOMY SYNDROMES

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77. Vogel SB, Hocking MP, Woodward ER: Clinical and radionuc1ide evaluation of RouxY diversion for postgastrectomy dumping. Am J Surg 155:57-62, 1988 78. Wilbur BG, Kelly KA: Effect of proximal gastric, complete gastric, and truncal

vagotomy on canine gastric electric activity, motility, and emptying. Ann Surg 178:295-302, 1973 79. Williams NS, Miller J, Elashoff J, et al: Canine resistances to gastric emptying of liquid nutrients after ulcer surgery. Dig Dis Sci 31:273-280, 1986 80. Woods 50S, Mitchell GJ: Delayed return of gastric emptying after gastroenterostomy. Br J Surg 76:145-148, 1989 81. Woodward ER, Hocking MP: Postgastrectomy syndromes. Surg Clin North Am 67:509-521, 1987

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