ENDOSCOPIC FEATURES OF GASTRODUODENAL CROHN'S DISEASE

GASTROENTEROLOGY 70:9-13, 1976 Copyright 1976 by The Williams & Wilkins Co. Vol. 70, No.1 Printed in U.S.A. ENDOSCOPIC FEATURES OF GASTRODUODENAL CROHN'S DISEASE JOSEPH T. DANZI, M.D., RICHARD G. FARMER, M.D., BENJAMIN H. SULLIVAN, JR., M.D., AND GEORGE B. RANKIN, M.D. The Department of Gastroenterology, The Cleveland Clinic Foundation, Cleveland, Ohio The clinical, roentgenographic and endoscopic findings in 14 patients with Crohn's disease of the stomach and/or duodenum are described. To date, this is the largest series of endoscopic findings of Crohn's disease of gastroduodenal region. The endoscopic findings include (1) l nodularity or "cobblestoned" ; (2) multiple aphthous-like ulcerations and/or linear ulcerations; (3) thickening of the antral folds; (4) antral narrowing with evidence of hypoperistalsis; (5) duodenal strictures. The diagnosis of gastric duodenal Crohn's disease is achieved by combining recognition of clinical features and roentgenographic and endoscopic features. The endoscopic features correlate well with the roentgenographic findings in our 14 patients. Tissue for histological diagnosis of Crohn's diseaf)e of the gastroduodenal area is rarely obtained by endoscopic biopsy, but peroral suction biopsy specimens may increase the rate of histological confirmation. Crohn's disease (transmural enteritis) can affect any part of the gastrointestinal tract. 1 Crohn's involvement of the stomach or duodenum, or both, is infrequent, 2, 3 but in the last decade, the recognition of gastroduodenal Crohn's disease has increased. ~ - 1 2 The roentgenographic features of Crohn's disease of the stomach and duodenum are outlined in many comprehensive reviews; 13-19 yet, there is limited data regarding the endoscopic features of gastroduodenal Crohn's disease. The endoscopic features described in case reports include: l nodularity, l erosions and ulcerations, antral narrowing, and thickened antral folds. 5-7, 9, 12 The diagnosis of Crohn's disease of the gastroduodenal area can be established in two clibical settings. Crohn's disease of the stomach and/or duodenum can occur in patients with documented Crohn's involvement of the small and/or large intestine. Crohn's disease of the gastroduodenal area can also occur as the initial area of involvement. A differential diagnosis of Crohn's disease of the stomach and/or duodenum, in both modes of occurrence, will be discussed. The diagnostic value of endoscopic biopsy in gastroduodenal Crohn's disease is not established. Roseman's report of a diagnostic endoscopic biopsy is the lone reported experience. 11 The histological diagnosis of gastroduodenal Crohn's disease by peroral suction biopsy technique has been reported. 20, 21 We describe the endoscopic features of 14 patients with gastroduodenal Crohn's disease. We correlate the Received April 11, 1975. Accepted July 18, 1975. This paper was presented at the American Society of Intestinal Endoscopy, May 21, 1975. Address requests for reprints to: Richard G. Farmer, M.D., The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, Ohio 44106. 9 endoscopic and roentgenographic features of these patients and comment on the diagnostic value of endoscopic biopsy. Methods and Materials From July 1965 to November 1975, 14 patients with Crohn's disease of the stomach and/or duodenum were examined. Endoscopy of the upper gastrointestinal tract was performed with the Hirschowitz 5001 fiberopticscope in 2 individuals. In both of these individuals, the stomach only was examined. One individual had endoscopic examination of the stomach performed with an Olympus GFC gastroscope. The remaining 11 patients had endoscopic examination performed with the Olympus GIF-D fiberoptic esphagogastroduodenoscope. In 10 of these individuals, both the stomach and duodenum were examined. In 1 individual, only the stomach was examined. The endoscopic observations were abstracted from the endoscopic report in each case. There were 10 males and 4 females ranging in age from 15 to 53 years (mean age, 32 years). Features concerning 1 patient with gastric Crohn's disease have been previously reported. 9 Clinical features. The areas of involvement with Crohn's disease included: (a) 3 patients with ileal and gastroduodenal Crohn's disease, (b) 9 patients with ileal, colonic, and gastroduodenal Crohn's disease, and (c) 2 patients with only gastroduodenal Crohn's disease. Both of these patients had duodenal Crohn's involvement only. The involvement of the gastroduodenal area with Crohn's disease included: (a) 7 patients with gastric and duodenal Crohn's disease, (b) 4 patients with only gastric disease, and (c) 3 patients had duodenal Crohn's disease alone. The mode of clinical presentation included: (a) 7 patients with upper gastrointestinal tract obstruction symptoms, (b) 6 patients with epigastric pain, and (c) 1 patient with occult upper gastrointestinal tract bleeding. Weight loss and postprandial vomiting were predominant features in patients with obstructive symptoms. Roentgenographic features. Twelve of 13 patients in whom

TABLE I. Patient Race Age and sex yr 15 WF 25 WM 22 WF 53 WF 32 WM 42 WM 21 WM 26 WM 20 WM 48 WM 46 WF 31 WM 47 WM 23WM Clinical Presentation Occult upper gastrointestinal bleeding Roentgenographic features DBa-spasm 2D-2-cm stricture Gastric distension A-decrease peristaltic activity; nodularity of DB2D-NL A-narrowed with nodular DB2D-nodular duodenal strictures in 2D No radiographs for review A-l nodularity; tubular antrum; T.A.F. D-NL DB-NL 2D-l nodularity; pseudo diverticulum 2D A-nodular ; ulceration of antrum DB2D-nodular and spasm A-mild l irregularities with A.U. DB2D-NL A-distended stomach, narrowed antropyloric area, l irregularity A-narrowing of antrum pylorus l nodularity DB 2D-l nodularity normal study DB2D-l nodularity, ulcerations with stricture of 2D A-l nodularity-antral/pyloric narrowing DB2D A-narrowed with nodular DB 2D-l nodular stricture (2 cm) in 2D Endoscopic observations DB-patchyerythema 2D-stricture circumferential; l nodularity adjacent to ulceration A-l nodularity; A.U.; decrease antral peristalsis; T.A. F.; L.U. in nodular DB2D-NL A-narrowed; T.A.F.; l nodularity; A.U. DB2D-l nodularity; duodenal stricture in 2D; L.U. adjacent to stricture DB-patchyerythema 2D-l nodularity; 6 cm distal to DB, a stenotic area A-cobblestoned ; A.U.; T.A.F. DB2D-NL DB-NL 2D-l nodularity; A.U. in nodular area pseudodiverticulum in 2D A-cobblestoned ; U.A. L.U. in cobblestoned ; T.A.F. DB2D-nodular ; L.U. in nodular A-nodular with A.U. in nodular NL A-nodular ; T.A.F.; narrowed antrum with pyloric obstruction A-Mucosal nodularity; A.U. L. U. in nodular ; narrowing of antrum; T.A.F. DB-l nodularity 2D-l nodularity-prominent folds A-l erythema with friability; multiple L.U. in normal DB2D-l erythema A-l nodularity DB2D-l nodularity; A.U. and L. U. in 2D; stricture of 2D A-l nodularity-narrowing of antrum-t.a.f. A-tubular antrum-l nodularity DB 2B-l nodular with stricture of 2D Other involve ment lc. 1 I, C Endoscopic biopsy Surgical confirmation Crohn's disease gastritis Crohn's disease DB, duodenal bulb; 2D, second portion of duodenum; A, antrum; A.U., aphthous-like ulceration; L.U., linear ulceration; T.A.F., thickened antral folds; I, ileal; C, colonic; NL, normal.

January 1976 ENDOSCOPIC FEATURES OF CROHN'S DISEASE 11 FIG. 1. Top illustrates the antral narrowing and l nodularity in a patient with gastric Crohn's disease. Bottom is the endoscopic photograph of the antrum of the same patient. The l nodularity is demonstrated and a whitish exudate-coated ulceration is demonstrated in the left midsection of the figure. the roentgenographic examinations were available for review had evidence suggesting Crohn's disease of the stomach and/or duodenum. The roentgenographic findings of each patient and the comparison of the roentgenographic features and endoscopic features are listed in table 1. illustrated roentgenograms and endoscopic photographs of selected cases are shown in figures 1 and 2. Endoscopic features. Patients with gastric Crohn's disease, alone or associated with duodenal Crohn's disease, had endoscopic evidence of Crohn's disease observed only in the antrum and pylorus. This endoscopic observation of the pattern of involvement in gastric Crohn's disease correlated with the roentgenographic findings. Patients with duodenal Crohn's disease alone had endoscopic features of Crohn's disease observed in the second and third portion of the duodenum, whereas those having associated gastric Crohn's disease had endoscopic evidence of disease in the first portion of the duodenum as well. The observed l abnormalities included: (1) l nodularity ("cobblestoning") in 13 of 14 patients, (2) multiple aphthous-like ulcerations in 9 of 14 patients, and linear or serpiginous ulcerations in 5 of those 9 patients with aphthouslike ulcerations. The aphthous-like and linear ulcerations were observed endoscopically to occur in cobblestoned and in normal appearing removed from the cobblestoned. Other endoscopic features included: (3) thickening of the antral folds in 7 of 11 patients with gastric disease, (4) antral narrowing in 3 of 7 patients with gastric and duodenal disease, and (5) duodenal stricture in 5 of 10 patients with duodenal disease. FIG. 2. Top is a roentgenograph of a patient with duodenal Crohn's disease in a nonstenotic phase. The abnormal thickened duodenal folds, "thumb printing," and segmental involvement of the duodenum are demonstrated. Bottom is the endoscopic photograph demonstrating the thickened nodular duodenum, with three stellate linear 11lcera tions. No patient had endoscopic evidence of duodenal bulb ulceration. Table 1 lists the endoscopic observations in each case. Figures 1 and 2 are illustrative endoscopic photographs of selected cases. Endoscopic biopsy. Nine endoscopic biopsies were performed in 9 patients during the endoscopic examination. Two biopsy specimens showed granulomatous compatible with Crohn's disease; these biopsy specimens were obtained from an ulcer base. Seven biopsies had chronic without evidence of noncaseating granuloma. Four specimens were obtained from an ulcer base, a n three ~ specimens were obtained from a nodular l segment. No peroral suction biopsy specimens were obtained in these patients. Discussion Crohn's disease of the gastroduodenal area occurring with documented ileal and/or colonic Crohn's disease must be differentiated from peptic ulcer disease. Incidence of peptic ulcer disease in patients with known Crohn's disease is reported to be increased, 22-24 but other investigators have not confirmed this view. 25-26 The localization of the peptic ulceration in the duodenal bulb (12 of 12 patients reported by Sanders and SchimmeP2 and 14 of 19 patients reported by Fielding and Cooke),23 appears an important differential point. of our 14 patients had either roentgenographic or endoscopic evidence of ulceration in the duodenal bulb. Endoscopic findings in a patient with peptic ulceration include l erythema and single or multiple ulcerations with gastric folds radiating toward the ulceration. The observed endoscopic features of gastroduodenal Crohn's

12 DANZI ETAL. Vol. 70, No. I disease allows for endoscopic differentiation from peptic ulceration. Crohn's disease with the stomach and/or duodenum occurring as the initial area of involvement poses other differential considerations. Eosinophilic gastritis, granulomatous gastritis, lymphoma of the stomach, and scirrhous carcinoma must be considered in the differential diagnosis. Patients with eosinophilic gastritis may present with obstructive symptoms and roentgenographically show antral or pyloric obstruction. Endoscopic findings of eosinophilic gastritis include hypoperistalsis of the antrum, small pyloric channel, and normal l appearance. 27 An endoscopic biopsy specimen will reveal the and sub to be infiltrated with eosinophi Is and plasma cells. Fahami et al. 28 have classified granulomatous gastritis into three groups: (1) associated with sarcoidosis, (2) associated with Crohn's disease, and (3) associated with primary granulomatous gastritis. Gastric sarcoidosis usually is associated with vague gastrointestinal symptoms and roentgenographic examination is typically normal. 29 The extra-intestinal sites of sarcoid involvement are usually clinically apparent. Endoscopic features and the histology of endoscopic biopsy specimens of gastric sarcoidosis are not stated in the literature. Primary granulomatous gastritis affects an older age group, patients between 60 and 80 years of age. Roentgenography will demonstrate an infiltrative process in the upper two-thirds of the stomach with a normal antrum in 40 % of the cases. 30 Cytological study may reveal multinucleated giant cells, and endoscopic biopsy may show granulomatous inf1ammation. The patient's age, the infiltrative nature of the lesion, and its isolated gastrointestinal occurrence make malignancy the main differential concern. Malignant lymphoma of the stomach could roentgenographically resemble Crohn's disease of the stomach; however, lymphoma of the duodenum is exceedingly rare. 31 The localization of Crohn's disease to the antrum and pylorus is a differential point in this case. Endoscopic biopsy and cytologic examination, especially the latter, are helpful in the preoperative diagnosis of gastric lymphoma. Scirrhous carcinoma of the stomach could roentgenographically show evidence of a narrowed non-motile antrum and pylorus. Endoscopic features include a non-motile gastric segment and loss of l folds, but the l pattern is normal. 32 Endoscopic biopsy is greater than 85% accurate in a diagnosis of gastric carcinoma. 32 There was good documentation of the roentgenographically observed l nodularity, antral narrowing, duodenal strictures, and thickened ant ral folds by endoscopy. Endoscopy demonstrated the aphthous-like and linear ulcerations not shown roentgenographically in patients with gastroduodenal Crohn's disease. Our experience with endoscopic biopsy for the histological confirmation of gastroduodenal Crohn's disease concurs with that in the literature. The superficial nature of the endoscopic biopsy make it difficult to obtain tissue which would be representative of a transmural disease, such as Crohn's disease. Colonoscopic biopsy specimens yield only a 50% histological confirmation rate. The use of peroral suction biopsy technique may give specimens allowing for the histological confirmation of the diagnosis of gastroduodenal Crohn's disease; however, further experience is necessary with this technique. REFERENCES 1. Dudney TP: Crohn's disease of the mouth. Proc R Soc Med 62:1237, 1969 2. Kusakcioglu 0, Norton RA : Granulomatous duodenitis, clubbed digits, and psoriasis: report of a case. Lahey Clin Found Bull 16: 191-193, 1967 3. Wilder, WM, Davis WD, Jr: Duodenal enteritis. South Med J 59:884-888, 1966 4. Farmer RG, Hawk WA, Turnbull RB, Jr: Crohn's disease of the duodenum (transmural duodenitis): clinical manifestations. Report of 11 cases. Am J Dig Dis 17:191-198, 1972 5. Wise L, Kyriakos M, McCown A, Ballinger W: Crohn's disease of the duodenum. Am J Surg 121 :184-194, 1971 6. Johnson FW, Delaney JP: Regional enteritis involving the stomach. Arch Surg 105:434-437, 1972 7. Beaudin D, Da Costa LR, Prentice RSA, Beck IT: Crohn's disease of the stomach: a case report and review of the literature. Am J Dig Dis 18:623-629, 1973 8. Laing RR, Dunn GD, Klotz AP: Crohn's disease of the stomach. Gastrointest Endosc 19:83-84, 1972 9. Elibol T, Rankin GB, Brown CH: Crohn's disease of the stomach. Gastrointest Endosc 14:201-204, 1968 10. Fielding JF, Toye DKM, Cooke WT: Crohn's disease of the stomach and duodenum. Gut 11 :1001-1006, 1970 11. Roseman DM: Crohn's disease of the stomach and duodenum: report of a case. Gastrointest Endosc 19:83-84, 1972 12. Haggett RC, Meissner WA: Crohn's disease of the upper gastrointestinal tract. Am J Clin Pathol 59:613-622, 1973 13. Farman J, Faegenburg D. Dallemand S, Chen CK: Crohn's disease of the stomach. Am J Roentgenol Radium Ther Nucl Med 123:242-251, 1975 14. Thompson WM, Cockrill H, Rice RP: Regional enteritis of the duodenum. Am J Roentgenol Radium Ther Nucl Med 123:251-261, 1975 15. Nelson SW: Some interesting and unusual manifestations of Crohn's disease (" regional enteritis") of the stomach, duodenum and small intestine. Am J Roentgenol Radium Ther Nucl Med 107:86-101, 1969 16. Bagby RJ, Rogers, JV, Jr, Hubbs C: Crohn's disease of the esophagus, stomach and duodenum: a review with emphasis on the radiographic findings. South Med J 65:515-523, May 1972 17. Marshals RH, Wolf BS: Roentgen findings in regional enteritis. Am J Roentgenol Radium Ther Nucl Med 74:1000-1014, 1955 18. Cohen WN: Gastric involvement in Crohn's disease. Am J Roentgenol Radium Ther Nucl Med 101:425-430,1967 19. Legge DA, Carlson HC, Judd ES: Am J Roentgenol Radium Ther Nucl Med 110:355-360, 1970 20. Hermos JA, Cooper HL, Kramer P, Trier JS: Histological diagnosis by peroral biopsy of Crohn's disease of the proximal intestines. Gastroenterology 59:868-873, 1970 21. Haner WV, Goldstein F, Wirto CW: Granulomas in suction biopsies of distal duodenum. Gastroenterology 59:862-867, 1970

January 1976 ENDOSCOPIC FEATURES OF CROHNS DISEASE 13 22. Sanders MG, Schimmel EM: The relationship between granulomatous bowel and duodenal ulcer. Am J Dig Dis 17: 1100-lJ07, 1972 23. Fielding JF, Cooke WT: Peptic ulcerations in Crohn's disease (regional enteritis). Gut 11:998-1000,1970 24. Fielding JF, Cooke WT, Williams JA: Gastric acid secretion in Crohn's disease in relation to disease activity and bowel resection. Lancet 1:1106-1107, 1971 25. Van Patte WN, Bargen JA, Dockerty MD, et al: Regional enteritis. Gastroenterology 26:347-450, 1954 26. Crohn BB, Yannis H: Regional enteritis. Second revised edition. New York, Grune and Stratton, 1958, p 46 27. N,avab F, Kleinman MS, Algazy K, Schenk E, Turner MD: Endoscopic diagnosis of eosinophilic gastritis. Gastroenterol Endose 19:67-69, 1972 28. Fahimi HD, Deren JJ, Gottlieb LS, Zamcheck N: Isolated granulomatous gastritis: its relationship to disseminated sarcoidosis and regional enteritis. Gastroenterology 45:161-175, 1963 29. Case records of N. Engl J Med 46, 1974. N. Engl J Med 291:1127-1133, 1974 30. Bruce RJ, Daber KS: Granuloma of the stomach. Br J Surg 46:379-382, 1959 31. Belber, JP: Gastroscopy and duodenoscopy, Ch. 41. In Gastrointestinal Disease. Edited by MH Sleisenger and JS Fordtran. Philadelphia, WB Saunders, 1973, p. 521-535 32. Brandborg LL: Polyps, tumors, and cancer of the stomach, Ch. 46. In Gastrointestinal Disease. Edited by MH Sleisenger and JS Fordtran. Philadelphia, WB Saunders, 1973, p 581-604