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Immunofluorescent Studies in Adult Celiac Disease

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Immunofluorescent Studies in Adult Celiac Disease Immunofluorescent Studies in Adult Celiac Disease Walter Rubin, … , Marvin H. Sleisenger, Graham H. Jeffries J Clin Invest. 1965;44(3):475-485. https://doi.org/10.1172/JCI105161. Research Article Find the latest version: https://jci.me/105161/pdf Journal of Clinical Investigation Vol. 44, No. 3, 1965 Immunofluorescent Studies in Adult Celiac Disease * WALTER RUBIN,t ANTHONY STEPHEN FAUCI, MARVIN H. SLEISENGER, AND GRAHAM H. JEFFRIES t WITH THE TECHNICAL ASSISTANCE OF SUE MARGOLIS (From the Department of Medicine, Cornell University Medical College, New York, N. Y.) The etiology of childhood and adult celiac dis- Two hypotheses of the mechanism of gluten ease is not known. It has been established, how- toxicity in celiac patients have been proposed ever, that gluten, a complex heterogeneous pro- (3). One hypothesis is that celiac disease is the tein in wheat and other cereal grains, plays a sig- result of an inborn error of metabolism-a defi- nificant role in the pathogenesis of the disease, and ciency of a specific peptidase in the intestinal mu- that the harmful factor resides in gliadin, the al- cosa, which results in the accumulation of indi- cohol soluble fraction of gluten (1-4). Treatment gestible toxic peptides of gliadin. Two recent of celiac disease with a gluten-free diet results in observations, however, have failed to demonstrate clinical and biochemical improvement usually ac- a specific peptidase deficiency in the small intes- companied by a decrease in the severity of the tinal mucosa of celiac patients (10, 11). pathologic lesion in the proximal small intestinal The second hypothesis suggests that celiac dis- mucosa. The ingestion of gluten by patients in ease may be immunologic: a local hypersensitivity remission on a gluten-free diet causes an exacer- reaction to gluten or to a gluten peptide. Several bation of symptoms, accompanied by malabsorption observations support this theory. Patients with and acute inflammatory changes in the proximal adult celiac disease often benefit clinically and jejunal mucosa (5). Furthermore, direct instil- biochemically from adrenocorticosteroid therapy lation of flour or gluten into the histologically (12). Celiac patients on a gluten-free diet have normal distal small intestine of patients with adult occasionally reacted dramatically to the ingestion celiac disease produces similar acute mucosal in- of minute quantities of gluten: such a response flammation (6), whereas the intestinal mucosa of has been called "gliadin shock" (13). The infil- a normal subject remains unchanged. The toxicity tration of the small intestinal mucosa in celiac of gluten and gliadin is retained by mixtures of disease with plasma cells, lymphocytes, macro- straight chain polypeptides that result from enzy- phages, and eosinophils is consistent with a local matic and chemical digestion of the protein (7-9). hypersensitivity reaction. In recent years, hu- Further digestion of these toxic peptides by fresh moral antibodies to wheat gluten and gluten frac- extracts of hog small intestinal mucosa or by tions have been found in the sera of both children crude papain renders them inactive (7, 8). De- and adults with celiac disease, in greater frequency amidation or complete acid hydrolysis of gliadin and titer than in normal controls. These anti- also renders it inactive (1). bodies have been demonstrated by complement fixation (14), immunodiffusion (15, 16), and *Submitted for publication August 24, 1964; accepted erythrocyte agglutination techniques (16-18). It November 27, 1964. is questionable, however, that humoral antigliadin Supported by the John A. Hartford Foundation and by are of etiologic importance in grant no. CA 09386 from the National Cancer Institute, antibodies primary U. S. Public Health Service. celiac disease, since celiac patients have also ex- t U. S. Public Health Service trainee, National Insti- hibited a higher incidence of humoral antibodies tute of Arthritis and Metabolic Diseases, grant no. TI to the milk proteins, casein, lactalbumin, and beta AM 5430. Address requests for reprints to: Dr. Walter lactoglobulin (15-18). Furthermore, there have Rubin, The New York Hospital-Cornell Medical Cen- ter, 525 East 68th St., New York, N. Y. 10021. been descriptions of acquired agammaglobuline- t U. S. Public Health Service Research Career De- mia in adult celiac disease (19). Skin tests to velopment Awardee, National Institute of Arthritis and gluten and its fractions have been negative in Metabolic Diseases, grant no. 5-K3-AM-14,153. celiac patients, and peripheral eosinophilia and a 475 476 RUBIN, FAUCI, SLEISENGER, AND JEFFRIES personal or family history of allergy are unusual Methods (2, 20). Duodenal and j ej unal biopsies were obtained with a Recent observations by Malik, Watson, Mur- peroral hydraulic multiple biopsy tube from nine patients ray, and Cruickshank (21) suggested the pres- with adult celiac disease (23). Two of these patients ence of a humoral autoantibody to small intestinal (D.R. and P.T.) had been undiagnosed previously and epithelium in untreated patients with adult celiac were untreated at the time of the study. In seven pa- disease. Using the indirect immunofluorescent tients, a diagnosis of adult celiac disease had been based on clinical and biochemical evidence of malabsorption technique, and a fluoresceinated antiserum to the and total villous atrophy of the proximal jejunal mu- human alpha and beta globulins, they demonstrated cosa, together with clinical and biochemical improve- a reaction between fresh sera from untreated celiac ment with a gluten-free diet. These patients had been patients and the cytoplasm of unfixed autologous on diet therapy for periods of 3 to 7 years. On careful questioning, however, only three of these seven patients jejunal mucosa, particularly in the crypts of had adhered strictly to the gluten-free diet; the other Lieberkuhn. They obtained similar results with four admitted to the regular ingestion of varying amounts homologous and even monkey jejunum. of gluten-containing foods. To investigate further the possibility that im- The biopsy specimens were embedded in 7.5% gelatin as described by Burkholder, Littell, and Klein (24), munologic processes play a role in the pathogene- were frozen within 1 to 3 minutes in an ice sis of adult celiac disease, duodenal and jejunal acetone-dry bath at - 70° C, and were stored at - 20° C in sealed biopsies from patients with adult celiac disease plastic bags to prevent dehydration. Other biopsy speci- were studied by immunofluorescent techniques. mens from each patient were fixed in 10%o neutral for- These studies were planned to determine: 1) malin, and paraffin sections were stained with hema- toxylin and eosin and with the periodic acid-Schiff whether immunoglobulins are present in these stains. Serum obtained from each patient was used tissues; 2) whether gliadin is bound by these im- immediately or stored at -20° C. munoglobulins or to any component of the in- Tests performed at the time of the biopsy study to testinal mucosa; 3) whether complement is fixed assess small intestinal function included chemical analysis in vivo in the mucosa as evidenced by the pres- of fat in a 3-day stool collection, and the measurement of 5-hour urinary excretion of D-xylose after a 25-g oral ence of of human com- beta,, globulin component dose. Table I summarizes the findings in each patient. plement (22) ; 4) whether immune complexes or The fecal fat absorption and D-xylose absorption had gamma globulin aggregates can be identified in returned to normal in the three patients who had fol- the tissues by their in vitro fixation of comple- lowed a strict gluten-free diet for periods of 3 to 5 ment both with or without preincubation with years. The j ej unal mucosa had returned to normal in one patient (K.D.), whereas in the other two patients gliadin; 5) whether an immunoglobulin in the (P.R. and J.T.), dissecting and light microscopy re- serum from celiac patients reacts with autologous vealed a leaf-like villous structure with persisting in- intestinal mucosa. flammatory cell infiltration. Of the four patients who TABLE I Celiac patients Duration Adherence to Fecal D-Xylose of symp- Duration of gluten-free fat absorp- Jejunal Patient Sex Age toms diet therapy diet excretion* tiont pathology yrs y5s 1. D.R. F 35 19 Untreated Untreated 29 2.4 Severe 2. P.T. M 55 5 Untreated Untreated 12.7t 3.6 Severe 3. R.C. F 49 23 7 No 13 6.3 Moderate 4. O.M. F 64 22 5 No 15 1.3 Moderate 5. W.S. M 32 29 5 No 4 5.4 Moderate 6. M.D. F 55 18 4 No§ 3 3.1 Mild 7. J.T. M 50 4 4 Yes 3 8.1 Mild 8. P.R. M 54 3 3 Yes 3 5.9 Mild 9. K.D. F 38 5 5 Yes 2 6 Normal * Grams per day from a 3-day stool collection. Normal is less than 5. t Grams excreted in 5-hour urine collection after ingestion of 25 g. Normal is greater than 4.0. t Collection obtained while the patient was on a low fat intake. § Patient was also on prednisolone, 12.5 mg per day. IMMUNOFLUORESCENT STUDIES IN ADULT CELIAC DISEASE 477 TABLE II A rabbit antigliadin antiserum was produced in the Control subjects following manner: 150 mg of gliadin2 was suspended in 1 ml of saline, thoroughly mixed with 1 ml of complete Patient Sex Age Diagnosis Freund's adj uvant,4 and inj ected intramuscularly into each of four female New 1. D.R. M 56 Scleroderma with steatorrhea Zealand white rabbits. Each 2. E.l. M 39 Regional ileitis rabbit received booster inj ections every 3 to 4 weeks. 3. B.S. M 66 Pancreatic steatorrhea They were bled 10 days after each injection, and their 4.
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