GLUTEN ENTEROPATHY APPEARING AFTER GASTRIC SURGERY
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1 GASTROENTEROLOGY 1966 by The Williams & Wilkins Co. Vol. 50, No.6 Printed in U.S.A. GLUTEN ENTEROPATHY APPEARING AFTER GASTRIC SURGERY C. ANDERSON HEDBERG, M.D., CLIFFORD S. MELNYK, M.D., AND CHARLES F. JOHl'iSON, M.D. Section of Gastroenterology, Department of Medicine, University of Chicago, Chicago, Illinois Diarrhea and weight loss occurring after gastric surgery may portend an undedying malabsorption syndrome. Explanation for such weight loss and diarrhea has focused upon mechanical factors related to the surgical procedure; the possibility of coexistent abnormalities in the small intestine has been minimized. Several gastric operative procedures are reported to be associated with steatorrhea of varying severity.1-3 The mechanism for postgastrectomy steatorrhea has been related to a disruption of intraluminal processes, including insufficient gastric digestion, asynchrony of food admixture with biliary and pancreatic secretions, and rapid intestinal transiu Information on small intestinal function in the post gastrectomy patient is limited, although studies utilizing radioactive labeled materials suggest that absorption is norma1. 5,6 The histology of the small intestinal mucosa is reported to be normal, or demonstrates only minor villous abnormalities or inflammatory changes which do not correlate with the presence or absence of steatorrhea. 7-9 In the literature, a few patients have been mentioned in whom small intestinal abnormalities appear to have contributed to postgastrectomy steatorrhea D escription of such patients has been incomplete, and reports on therapy are not available. Weare reporting the clinical, pathological, Received December 21, Accepted February 4, Address requests for reprints to: Dr. Charles F. Johnson, Section of Gastroenterology, Department of Medicine, University of Chicago, 950 East 59th Street, Chicago, Illinois This study was supported in part by Grants TI-AM and AM from the National Institutes of Health, Bethesda, Maryland. 796 and therapeutic features of four patients in whom diarrhea and weight loss appeared after gastric surgery. A primary defect in the small intestine causing severe malabsorption was demonstrated. In each instance, a dramatic improvement occurred upon the institution of a gluten-free diet. Case Reports The results of laboratory studies before and after treatment are given in table 1. Figure 1 portrays changes in body weight. Case 1: G. A. ( ), 45-year-old white man. In February 1958 this patient underwent a 60% gastrectomy and a Billroth II anastomosis for a benign gastric ulcer. Immediately after surgery, he noted a change from his normal bowel habit to 8 to 12 malodorous, greasy, floating stools per day. He lost 28 kg in weight and had episodes of tetany. Upon institution of a diet with partial restriction of gluten, he gained 13 kg but continued to have occasional diarrhea, and he could not regain his preoperative weight. He was hospitalized at the University of Chicago Hospital in March Physical examination revealed a thin, chronically ill, white man who weighed 58 kg. Significant findings included scaly skin, a distended abdomen, and ankle edema. A small bowel X ray showed coarse mucosal folds, with clumping of barium. Peroral jejunal mucosal biopsy (fig. 2A) demonstrated villous atrophy, with submucosal infiltration of plasma cells and lymphocytes. On a strict gluten-free diet, he gained an additional 15 kg in 3 months. A recurrence of diarrhea and weight loss in 1962 responded to dietary reinforcement. A second jejunal mucosal biopsy in April 1965 (fig. 2B) demonstrated villous formation with a less prominent inflammatory cellular infiltrate. At the present time, the patient is asymptomatic. Comment: This patient had normal bowel habits prior to gastric surgery. Postoperative diarrhea and weight loss were dramatic, the loss amounting to 40% of the preoperative
2 June 1966 GLUTEN ENTEROPATHY AFTER GASTRIC S URGERY 797 TABLE 1. LaboratoTY da ta befote and aflej' ttealmen! with a gluten-free diel Case and date Plasma Hematocrit Calcium albumin- Cholesterol Carotene Xylose Schilling Stool fat (40-47)" \9-11 ) globulin ( ) ) (>5 g/5 hr) (>7) «5 g/ day) (4--5.5/2-2.5) % mg/ JOO.. I g/loo Inl mg/ioo ml p.g/ml g/s hr % excreted g/day Case 1 (G.A.) 3/ / b / / Case 2 (C.T.) 4/ / / /3.7 Case 3 (M.S. ) 6/ / ' 51 4/ / , Case 4 (M.J.) 10/ / O. Jb 16 7/ / I Values given in parentheses in the boxheads are the n ormal r anges. b No correction with int rinsic factor., N o correction with intri nsic factor or following oral tetracycline for 5 days. FIG. 1. The changes in body weight occurring postoperatively and after a gluten-free diet are depicted for each case. weight. The biopsies, clinical response to a gluten-free diet, and the symptomatic relapses on exposure to gluten indicate a diagnosis of gluten enteropathy which first appeared after the surgery. Case 2 : G. T. ( ), 37-year-old white man. This patient had occasional episodes of distention and diarrhea, with odiferous, light colored stools, and a gradual weight loss of 14 kg from 1956 to In January 1962 a gastroenterostomy and vagotomy were performed for a duodenal ulcer. Postoperatively, severe, persistent diarrhea developed, with weakness, leg pains, ankle e dema, and a 14-kg weight loss
3 798 HEDBERG ET AL. Vol. 50, No.6 FIG. 2. A, Pretreatment jejunal mucosal biopsy of case 1 (G. A.), demonstrating absence of villi, elongation of crypts, and an infiltration of the interstitium with large numbers of round cells (H & E, X 125). B, Biopsy obtained 24 months after institution of a gluten-free diet reveals the presence of abnormal villi and a continuing infiltration with large numbers of round cells (H & E, X 125). over a 4-month period. On admission to the University of Chicago Hospital in April 1962, physical examination revealed a malnourished white male who weighed 49 kg. Small bowel X-rays demonstrated marked segmentation of the barium with moderate dilation of multiple segments. Bone X-rays revealed diffuse de- mineralization. Peroral jejunal mucosal biopsy (fig. 3A) demonstrated villous atrophy with a marked infiltrate of plasma cells. Institution of a gluten-free diet resulted in a prompt response, with one to two well formed bowel movements per day, and a weight gain of 22 kg in 9 months. Repeat jejunal mucosal biopsies in
4 June 1966 GLUTEN ENTEROPATHY AFTER GASTRIC SURGERY 799 FIG. 3. A, Pretreatment jejunal mucosal biopsy of case 2 (G. T.) demonstrates shortened, thickened, and clubbed villi which are diminished in number. The prominent round cdl infiltration of the interstitium consists of plasma cells predominantly (H & E, X 80). B, Biopsy obtained after 30 months of a gluten-free diet reveals the presence of villi which are irregularly arranged, and often abnormally shaped. The inflammatory cell infiltrate is diminished (H & E, X 125) and 1964 (fig. 3B) have revealed progressive improvement in villous structure and a decrease in inflammatory cellular infiltrate. The patient is presently asymptomatic. Comment: After a gastroenterostomy and a vagotomy, an operation which is rarely followed by severe weight loss, diarrhea and a 14-kg weight loss rapidly occurred. Symptoms of intermittent distention and diarrhea with a gradual weight loss were present for 7 years prior to the surgery. The response to a glutenfree diet has been excellent.
5 800 HEDBERG ET AL. Vol. 50, No.6 Case 3: M. S. ( ), 46-year-old white woman. During infancy, this patient had distention and diarrhea, and failed to thrive. The symptoms regressed spontaneously in childhood, and she developed normal bowel habits. She attained an average adult weight of 57 kg. A cousin was said to have developed "adult sprue." In February 1964 a 40% subtotal gastrectomy with Billroth II retrocolic anastomosis was performed as treatment for a duodenal ulcer. One week after surgery, diarrhea characterized by 10 bowel movements per day of odiferous, floating stools developed. Two months after surgery she noted nausea, right upper quadrant fullness, and bilious vomiting 1 to 2 hr after meals. She lost 11 kg during a 4- month period. On admission to the University of Chicago Hospital in June 1964, the patient was a pale, cachectic, white woman weighing 45 kg. Pretibial edema was present. Upper gastrointestinal X-rays showed a Billroth II anastomosis and prolonged retention of barium in a large afferent loop. A small bowel X-ray showed coarse mucosal folds with dilation of the bowel and segmentation of barium. Two jejunal mucosal biopsies (fig. 4A) demonstrated villous atrophy with a marked infiltration of chronic inflammatory cells. Assays of these specimens revealed a pronounced depression of sucrase, lactase, and maltase. At surgery, a long afferent loop was found and corrected by a Billroth I reconstruction. Following surgery, the vomiting cleared but the diarrhea and steatorrhea persisted. A gluten-free diet then was instituted, with a prompt response. Reevaluation in April 1965 revealed an asymptomatic patient who had gained 14 kg over the previous 7-month period. A repeat jejunal mucosal biopsy (fig. 4B) demonstrated a broadened and irregular villous structure and the persistence of an inflammatory cell infiltrate in the lamina propria. Disaccharidase assays showed normal sucrase and maltase levels, but a continuing lactase deficiency. Comment: This patient had a history in childhood compatible with celiac disease, with spontaneous remission. Evidence of malabsorption again appeared after a Billroth II gastrectomy. The correction of an afferent loop obstruction did not substantially lessen the steatorrhea, which, however, responded excellently to a gluten-free program. Abnormalities in the jejunal mucosal histology and a minor elevation of fecal fat persist after 7 months of therapy. Case 4: M. J. ( ), 48-year-old white woman. In January 1964 a simple gastroenterostomy was carried out for duodenal ulcer. Following surgery the patient passed 8 to 10 watery bowel movements per day, and rapidly lost 15 kg. Reexploration in May 1964 revealed an afferent loop obstruction secondary to marginal ulceration, and an enteroenterostomy was performed. Because of persistent diarrhea and weight loss, she entered the University of Chicago Hospital in October Physical examination demonstrated a cachectic, chronically ill, white woman weighing 30 kg. The liver was enlarged 5 em below the costal margin, and there was a positive Trousseau's sign. An upper gastrointestinal X-ray showed a functional gastroenterostomy and an enteroenterostomy. A small bowel X-ray revealed dilated loops with flocculation of the barium mixture. At surgery normal gastroduodenal continuity was restored. Biopsies of the small intestine (fig. 5) demonstrated villous atrophy of the jejunum and inflammatory infiltration of the jejunum and ileum. A glutenfree diet was instituted, but persistent vomiting led to reexploration in June A partial obstruction from adhesions at the ligament of Treitz was corrected. In the subsequent 4 months she has responded to the gluten-free diet with a decrease in diarrhea and weight gain. Comment: Three operations were carried out following an inadequate surgical procedure for duodenal ulcer disease. Despite restoration of normal gastroduodenal continuity, institution of a gluten-free diet was necessary for symptomatic improvement and weight gain. Discussion Persistent weight loss or failure to regain the preoperative weight, often accompanied by diarrhea, may negate the success of gastric surgery. Considerable investigation of patients with these complications has produced a variety of explanations for the causative mechanisms. 4 W e have found four patients who developed a postoperative malabsorption syndrome with histology of the small intestinal mucosa and response to a gluten-free diet which were diagnostic of gluten enteropathy. All of the patients were cachectic and undoubtedly had a potentially fatal illness. The most striking clinical feature was the immediate and profound weight loss following surgery; in all cases the loss exceeded 20% of the preoperative weight. Mechanical complications in cases 3 and 4 contributed to the weight loss, but were not solely
6 June 1966 GLUTEN ENTEROPATHY AFTER GASTRIC SURGERY 801 FIG. 4. A, Pretreatment jejunal mucosal biopsy of case 3 (M. S.) demonstrates shortened and thickened villi. The crypts are tortuous and elongated. A considerable inflammatory cell infiltrate is present (H & E, X 80). B, Biopsy obtained after 7 months of a gluten-free diet reveals the appearance of abnormal villi which are shortened, thickened, and irregularly arranged. The infiltration with inflammatory cells is only slightly diminished (H & E, X 125). causative. Following P61ya gastric resection, most patients have difficulty regaining their preoperative weight; however, a weight loss of greater than 20% is unusual. Anderson et al. 12 documented weight loss to this degree in only 2.2% of males and 9.8% of females who had this procedure. Most patients who have a gastroenterostomy and a vagotomy without gastric re- fection maintain an adequate weight after the procedure. Cox et al. 13 found weight loss in only 28 of 93 patients after this operation, and a loss greater than 15 kg in only three patients. Our case 2, however, lost 14 kg, or 22% of his preoperative weight, following this procedure. Rapid and excessive weight loss following any type of gastric surgery should raise the possi-
7 802 HEDBERG ET AL. Vol. 50, No.6 FIG. 5. Pretreatment jejunal mucosal biopsy of case 4 (M. J.) demonstrates absence of villi, elongation of the crypts, and an infiltration of inflammatory cells (H & E, X 80). bility of malabsorption syndrome secondary to a small intestinal abnormality. The laboratory features of these cases which are characteristic of malabsorption syndrome merit discussion. Anemia and steatorrhea are nonspecific findings in the diagnosis of the cause of malabsorption, and are demonstrable in postgastrectomy patients without other detectable abnormalities. 9 The xylose tolerance test was abnormal in the three patients tested in this report. This test is invariably abnormal in untreated symptomatic sprue, but is usually normal in the postgastrectomy patient. 14, 15 However, lowered xylose absorption has been encountered occasionally in postgastrectomy patients with and without steatorrhea. 16,17 The explanation for this finding is not clear, but "intestinal hurry" is a possible mechanism. The small bowel radiological findings compatible with malabsorption syndrome, including dilation, segmentation, and coarsened mucosal folds, were seen in all of our patients. Patients who have had a gastrectomy and vagotomy may demonstrate similar abnormalities, but usually these changes are transient and less severe. 18 The diagnosis of gluten enteropathy includes the demonstration of partial or subtotal villous atrophy in a biopsy specimen of the small bowel. The small intestinal mucosa is often histologically normal in postgastrectomy patients; however, slight abnormalities in villous structure and mild inflammatory changes have been described. 7,8 More recently, increased numbers of leaflike villi, detectable with the dissecting microscope, have been reported. 9 These mild changes do not correlate with the presence or absence of postoperative steatorrhea. The appearance of atrophic villous changes of a degree seen in untreated gluten enteropathy is an unusual finding in the postgastrectomy patient. Investigators who have discussed such patients have speculated that they may represent a combination of gluten enteropathy and a postgastrectomy state. 9, 19 All four of our patients demonstrated a severe degree of mucosal flattening with no villous formation and a prominence of a cuboidal epithelium. Large numbers of round cells, including plasma cells and lymphocytes, were present in the lamina propria. In one instance (case 3), a marked diminution in mucosal disaccharidase activities was also demonstrated. Changes of this advanced degree, although not specific for gluten enteropathy, are typical of this disease in the adult. 20 The histological appearance returned toward normal in cases 1, 2, and
8 June 1966 GLUTEN ENTEROPATHY AFTER GASTRIC SURGERY concurrently with symptomatic Improvement on the gluten-free diet. In retrospect, the histories of these patients contain some clinical clues which should have aroused the suspicion preoperatively that a latent small bowel disease existed, and should have led to appropriate evaluation before the gastric surgery was undertaken. These include: a childhood history of celiac disease or a family history of sprue, episodic or chronic diarrhea, weight loss, or suboptimal weight. In our series, case 3 had a childhood history suggestive of celiac disease and a family history suggestive of sprue. Case 2 had episodic diarrhea, with gradual weight loss, for several years prior to gastric surgery, and case 4 was a thin woman who never weighed more than 45 kg. In contrast, case 1 preoperatively was an entirely asymptomatic man of average height and weight. These facts suggest that cases 2, 3, and 4 had small bowel disease prior to their gastric operation. The surgical disruption of normal intraluminal digestive processes superimposed on small bowel disease may have precipitated the overt expression of the malabsorption syndrome. SUllllllary Four patients with severe malabsorption syndrome precipitated by gastric surgery are described. The clinical features were diarrhea, steatorrhea, and a dramatic weight loss promptly following surgery. Laboratory determinations were consistent with malabsorption syndrome. Small intestinal mucosal biopsy demonstrated villous atrophy and inflammatory cell infiltration. In each instance, a gluten-free diet led to clinical improvement and a return toward normal of the laboratory meassures of absorptive function. The appearance of the proximal intestinal mucosal histology improved in 3 cases. These findings indicate that evaluation of small bowel function should be undertaken prior to gastric surgery in patients with a family or past history of celiac disease, or symptomatology suggestive of an absorptive defect. Furthermore, this study emphasizes the importance of adequate evaluation of the small intestine in patients with steatorrhea following gastric surgery. Although malabsorption in the postgastrectomy patient may result from disruption of intraluminal digestive processes, the recognition of a concomitant gluten enteropathy can lead to lifesaving dietary therapy. REFERENCES 1. Lawrence, W., P. Vanamee, A. S. Peterson, G. McNeer, S. Levin, and H. T. Randall Alterations in fat and nitrogen metabolism after total and subtotal gastrectomy. Surg. Gynec. Obstet. 110: Wollaeger, E. E., M. W. Comfort, J. F. Weir, and A. E. Osterberg The total solids, fat and nitrogen in the feces. II. A study of persons who had undergone partial gastrectomy with anastomosis of the entire cut end of the stomach and the jejunum (Polya anastomosis). Gastroenterology 6: Butler, T. J., and R. D. Eastham Absorption studies after gastrojejunostomy with and without vagotomy. Gut 6: Lundh, G The mechanism of postgastrectomy malabsorption. Gastroenterology 42: Barker, H., L. R. MaIm, and K. Reemtsma Study of fat and fatty acid absorption in postgastrectomy patients using radioactive labeling. Xew York J. Med. 60: Shingleton, W. W., J. K. Isley, R. D. Floyd, A. P. Sanders, G. J. Baylin, R. W. Postlethwait, and J. M. Ruffin Studies on postgastrectomy steatorrhea using radioactive triolein and oleic acid. Surgery 42: Baird, 1. M., and O. G. Dodge Jejunal biopsy after partial gastrectomy. Quart. J. Med. 26: Lees, F., and L. C. Grandjean The gastric and jejunal mucosa in healthy patients with partial gastrectomy. A. M. A. Arch. Intern. Med. 101: Scott, G. B., M. J. Williams, and C. G. Clark Comparison of jejunal mucosal in postgastrectomy states, idiopathic steatorrhea, and controls using the dissecting microscope and conventional histological methods. Gut 5: Paulley, J. W., F. A. Fairweather, and A. Leming Postgastrectomy steatorrhea and patchy jejunal atrophy. Lancet 1: Joske, R. A., and J. B. Blaekwell Alimentary histology in the malabsorption
9 804 HEDBERG ET AL. Vol. 50, No.6 syndrome following partial gastrectomy. Lancet 2: Anderson, C. D., R. T. S. Gunn, and J. K. Watt Results of partial gastrectomy in treatment of peptic ulcer. Brit. Med. J. 1: Cox, A. G., M. R. Bond, D. A. Podmore, and D. P. Rose Aspects of nutrition after vagotomy and gastrojejunostomy. Brit. Med. J. 1: Butterworth, C. E., Jr., E. Perez-Santiago, J. Martinez De Jesus, and R Santini Studies on the oral and parenteral administration of d-xylose. New Eng. J. Med. 261: Finlay, J. M., J. Hogarth, and K. J. R Wightman A clinical evaluation of the d-xylose tolerance test. Ann. Intern. Med. 61: Rinaldo, J. A., Jr Interrelation of tests of intestinal absorption. Gastroenterology 40: Benson, J. A., Jr., P. J. Culver, S. Ragland, C. M. Jones, G. D. Drummey, and E. Bougas The d-xylose absorption test in malabsorption syndromes. New Eng. J. Med. 256: Marshak, R H., B. S. Wolf, and D. Adlersberg Roentgen studies of the small intestine in sprue. Amer. J. Roentgen. 72: Illingworth, C. F. W Postgastrectomy syndromes; a review. Gut 1: Collins, C. R, and K. J. Isselbacher The occurrence of severe small intestinal mucosal damage in conditions other than celiac disease (nontropical sprue). Gastroenterology 49:
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